Annals of Botany 104: 557 –563, 2009
doi:10.1093/aob/mcn191, available online at www.aob.oxfordjournals.org
Oeceoclades maculata, an alien tropical orchid in a Caribbean rainforest
Ian M. Cohen1,* and James D. Ackerman2
1
Institute for Tropical Ecosystem Studies, University of Puerto Rico, PO Box 23341, San Juan, Puerto Rico 00931-3341, USA
and 2Department of Biology, University of Puerto Rico, PO Box 23360, San Juan, Puerto Rico 00931-3360, USA
Received: 26 March 2008 Returned for revision: 28 April 2008 Accepted: 14 July 2008 Published electronically: 7 October 2008
† Background and Aims Undisturbed forest habitat can be relatively impenetrable to invasive, non-native species.
Orchids are not commonly regarded as invasive, but some species have become invasive and these generally
depend on habitat disturbance. One of the most aggressive orchids is Oeceoclades maculata, a terrestrial
species with remarkable ecological amplitude. Originally from tropical Africa, it is now widespread in the
neotropics. By associating its local distribution with land-use history and habitat characteristics, it was determined whether O. maculata is dependent on habitat disturbance. It was also investigated whether this exotic
orchid occupies the same habitat space as two sympatric native species.
† Methods Six 10 m 500 m transects were censused in June 2007 on the 16-ha Luquillo Forest Dynamics Plot,
located in the Luquillo Mountains, Puerto Rico. The plot had been mapped for historical land use, topography
and soil type.
† Key Results Oeceoclades maculata was the most abundant of three orchid species surveyed and was found in all
four historical cover classes. In cover class 3 (50–80 % forest cover in 1936), 192 of 343 plants were found at a
density of 0.48 plants per 5 5 m subplot. Over 93 % of the 1200 subplots surveyed were composed of Zarzal or
Cristal soil types, and O. maculata was nearly evenly distributed in both. The orchid was most common on relatively flat terrain. The distribution and abundance of two sympatric orchid species were negatively associated
with that of the invasive species.
† Conclusions Oeceoclades maculata does penetrate ‘old growth’ forest but is most abundant in areas with moderate levels of past disturbance. Soil type makes little difference, but slope of terrain can be important. The negative association between O. maculata and native species may reflect differences in habitat requirements or a
negative interaction perhaps at the mycorrhizal level.
Key words: Oeceoclades maculata, Wullschlaegelia calcarata, Prescottia stachyodes, Orchidaceae, land-use
history, tropical forest disturbance, terrestrial orchids, invasive species, Luquillo Experimental Forest, Puerto
Rico, forest recovery, Caribbean.
IN T RO DU C T IO N
Spread of invasive species has become a global concern with a
wide array of opinions on what, if any, actions should be taken
to remove them from the landscape (Ewel and Putz, 2004;
Lugo, 2004; Denslow and Johnson, 2006). Success of many
invasive species can be directly tied to previous land-use
history such as agriculture and logging, which open up seemingly impenetrable landscapes (Costa and Magnusson,
2002; Sax et al., 2002; Grau et al., 2003; Lindborg and
Eriksson, 2004; Flinn and Velland, 2005). Abandonment of
these radically altered lands, generally due to economic
shifts, leaves open disturbed areas that are easily colonized
by non-native species (Aide et al., 2000; Lugo, 2004). This
may be particularly true for tropical islands where naturalized
exotic plant species have approximately doubled the size of
some floras (Sax et al., 2002; Denslow, 2003; Denslow and
Johnson, 2006; Gimeno et al., 2006) and where the frequency
of introductions is high (Lockwood et al., 2007).
The islands of the Caribbean have a long history of ecological disturbance and recovery, both from natural and human
* For correspondence. Present address: Department of Biological and
Environmental Sciences, 215 Holt Hall, 615 McCallie Avenue, Chattanooga,
TN 37403, USA. E-mail [email protected]
causes. Most of the Caribbean is subjected to the destructive
power of hurricanes, but the most dramatic ecological alteration that has occurred since the 15th century has been the
arrival of Europeans. In Puerto Rico, the landscape went
from nearly 100 % forest cover to ,6 % by the 1940s (Aide
et al., 2000; Rudel et al., 2000; Lugo, 2004). In the years
that followed, an exodus from rural farms to urban factories
occurred as the island economy shifted to one more reliant
on small industry. Abandoned farms were allowed to become
secondary forests to such an extent that ‘from 1950 to 1990
proportionally more land in Puerto Rico had been reforested
than anywhere in the world’ (Rudel et al., 2000). Although
this transformation is currently unusual, it may portend
changes elsewhere in the tropics as economies evolve
worldwide.
Luquillo Experimental Forest of Puerto Rico was established in the 1930s and at the time consisted of a mosaic of
land uses. It is now entirely forested, but variation in human
use at the time of establishment has had a great effect on
current tree species composition. Nevertheless, the forest is
sufficiently mature to become largely impenetrable to nonnative invasive tree species (Thompson et al., 2002).
Herbaceous components of its understorey vegetation also
show patterns of abundance associated with historical land
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558
Cohen & Ackerman — Land use and orchid onvasiveness
use (Portugal Loayza, 2005; Bergman et al., 2006), but it is not
known how impenetrable the forest is to invasion by nonnative herbaceous species.
Here, ecological correlates of distribution and abundance of
an invasive, terrestrial orchid, Oeceoclades maculata are
examined in the Luquillo Mountains of Puerto Rico. The
species was first described from Brazil in 1829. It is thought
to have originated in the tropical regions of Africa because it
is the only species in the genus that exists outside of Africa,
Madagascar and several small adjacent islands (Dod, 1986;
Stern, 1988). Today, O. maculata is found throughout the
neotropics, making it one of the most successful invasive
plant species (Dod, 1986; Stern, 1988). The species is autogamous, at least in Puerto Rico, which may help explain its
march through the neotropics (González-Dı́az and Ackerman,
1988). Among invasive orchids, reproductive systems vary
from apomixis and autogamy to obligately outcrossing
systems with deceptive pollination systems (Ackerman,
2007). Autogamy, then, is not likely to be the sole reason
for the success of O. maculata.
Oeceolades maculata was first noted in Puerto Rico in the
mid 1960s and has rapidly spread throughout the island
(González-Dı́az and Ackerman, 1988). Based on the definitions of Richardson et al. (2000), it is both invasive and naturalized. The species occurs in a wide range of habitats from
the northern mogotes (karst hills), where it is most abundant
in the moist to wet understorey of secondary forests, to the
southern dry forests of Guánica (González-Dı́az and
Ackerman, 1988). The rainforest of the Luquillo Mountains is
one of the last areas of Puerto Rico to be invaded by
O. maculata; the first collection was made in 1987 (Ackerman
2384, UPRRP). Here it is investigated how land-use history
may be associated with the distribution of invasive
O. maculata, particularly whether the orchid has established
in old-growth habitats. Potential effects of other ecological conditions such as soil type and slope of the terrain are explored
further. Finally, the relationship between distributions of
native terrestrial orchids in the forest and that of O. maculata
are examined.
M E T H O DS
Species
A census of three species of Orchidaceae was conducted with
the primary focus being on the distribution of the invasive
Oeceoclades maculata (Lindl.) Lindl. Wullschlaegelia calcarata Benth. and Prescottia stachyodes (Sw.) Lindl. were
assessed to establish the current relationships with
O. maculata and provide a baseline to determine if the invasive
species will have an effect on their distributions in years to
come. All three have minute, dust-like, wind-dispersed seeds
typical of the family. They are also entirely dependent on
mycorrhizal associations for successful seed germination.
Voucher specimens for the three species were deposited at
the University of Puerto-Rı́o Piedras herbarium (UPRRP;
O. maculata: Cohen 169; P. stachyodes: Cohen 170;
W. calcarata: Cohen 171).
Oeceoclades maculata is found in shaded, often disturbed
habitats ranging from dry to wet forests and from sea level
to 750 m throughout Puerto Rico but is most abundant in the
northern karst region. Plants are sympodial and caespitose
with short pseudobulbs, and each shoot bears one to three distinctively mottled green leaves. Inflorescences arise from the
base of pseudobulbs (Ackerman, 1995). Flowers are autogamous but less than half produce fruit. Fruit production is
resource limited (González-Dı́az and Ackerman, 1988).
Wullschlaegelia calcarata is a saprophytic, achlorophyllous
orchid found in the understorey of tropical rainforests of the
West Indies, Central America and South America (Born
et al., 1999). It grows in the montane forests of Puerto Rico
between 250 m and 750 m (Ackerman, 1995) where densities
may reach over 1300 plants ha21 (Bergman et al., 2006). A
single, erect, leafless shoot arises from a cluster of short fusiform roots embedded in partially decomposed leaf litter or
just below the soil surface. The whitish plants reach a height
of 15–55 cm and have a racemose inflorescence of several to
many, cleistogamous flowers. The small fruits mature rapidly
(Ackerman, 1995).
Prescottia stachyodes is a terrestrial orchid (rarely rupicolous or epiphytic) of variable size, often .50 cm tall, found
in the understorey of wet forests in Brazil, Venezuela,
Colombia, Central America, Mexico and the West Indies. In
Puerto Rico it occurs in moist to wet montane forests
between 450 m and 800 m elevation (Ackerman, 1995)
where densities may reach 960 plants ha21 (M. Whitman
and J. Ackerman, unpubl. res.). Plants have shallow, thick,
fleshy roots produced from a short, rhizome. The few persistent, basal leaves are elliptical and dark green to dark purplish
green. The erect inflorescence produces numerous flowers in a
dense raceme. In Brazil, flowers are pollinated by pyralid
moths (Singer and Sazima, 2001). Pollinators and breeding
system are unknown in Puerto Rico, but morphological examination of flowers along the inflorescence axis suggests that
autogamy is likely (A. Cuevas, pers. comm.). Fruit set generally approaches 100 % (Ackerman, 1995).
Study site
Field work took place on the 16-ha Luquillo Forest
Dynamics Plot (LFDP, south-west corner 188200 N,
658490 W), which is near El Verde Field Station (University
of Puerto Rico) in the Luquillo Mountains. The site lies
within the subtropical wet life-zone (Holdridge system; Ewel
and Whitmore, 1973) and averages approx. 3500 mm of rainfall annually (at least 200 mm per month), with March and
April being the driest months (Thompson et al., 2002). The
LFDP is in the north-western part of the 19 648-ha Luquillo
Experimental Forest and is approx. 1.2 km from the nearest
forest boundary and ranges in elevation from 333 m to
425 m (Thompson et al., 2002). It was divided into four
hundred 20 m 20 m plots, each of which was further subdivided into sixteen 5 m 5 m subplots.
Thompson et al. (2002) mapped the LFDP into four canopy
cover classes based on historical records including aerial
photographs from 1936. Today, the current canopy coverage
is nearly 100 % in the LFDP, but effects of previous land
use can still be seen today in the composition and distribution
of tree species (Thompson et al., 2002). Canopy cover classes
are as follows: cover class 1 (1.16 ha, ,20 % canopy cover),
Cohen & Ackerman — Land use and orchid invasiveness
cover class 2 (3.96 ha, 20 – 50 % canopy cover), cover class 3
(5.64 ha, 50– 80 % canopy cover). These first three cover
classes comprise the northern half of the LFDP; they were
all logged and used for various agricultural activities including
coffee, mangos and bananas. Canopy class 4 (5.24 ha, .80 %
canopy cover) makes up the southern portion of the LFDP and
was never clear-cut or used for agriculture, but it was subject
to some selective logging in the 1940s.
Cover classes and orchid distribution
To determine the association of land-use history and distribution and abundance of O. maculata within the LFDP, six
500-m transects running south to north were made crossing
into the historic canopy cover classes. Each transect was 10 m
wide (two adjacent 5 m 5 m subplots) with 30 m between
each transect except for transects 1 and 6 which were 15 m
from the eastern and western boundaries of the LFDP.
Because the LFDP is representative of the surrounding forest,
transects 1 and 6 suffer no edge effect. Twelve hundred
5 m 5 m subplots were surveyed to measure abundance of
the three orchid species during June 2007.
Neither Prescottia stachyodes nor O. maculata was in flower
at the time of survey, but they were easily identified using leaf
characters. Plants of both species are easily spotted in the
forest in the non-flowering condition because the leaves are
the most conspicuous part of the plants. Wullschlaegelia calcarata was past flowering but, during the study, shoots were still
visible as capsules were maturing and dispersing seed. Plants
of W. calcarata are only visible when inflorescences or infructescences are present. To enhance independence among subplots for statistical analyses, 100 of 101 subplots from cover
class 1 and 100 subplots from the three other cover classes
were randomly selected. It was investigated whether abundance
of O. maculata was associated with any of the four classes of historical canopy coverage using the nonparametric Kruskal–
Wallis test to compare numbers of orchids per subplot and
obtain a comparison among means. It was also examined
whether frequency of plots with at least one O. maculata plant
was independent of cover class using a chi-square test of independence. These and all other analyses were performed using
the statistical package JMP (version 4.04; SAS Institute, Cary,
NC, USA).
Soil type, slope of terrain and orchid distribution
The association of O. maculata, W. calcarata and
P. stachyodes with soil type and slope of the terrain in the
LFDP was measured using the nonparametric Kruskal–
Wallis test. Soil and slope analyses were done using soil
maps from the US Department of Agriculture soil survey
(Soil Survey Staff, 1995). The soil data are based on 20 m 20 m plots and were interpolated for each of the 5 m 5 m
subplots that make up a 20 m 20 m plot. The LFDP is separated into five major soil types: Zarzal, Prieto, Cristal, Coloso
and Fluvaquents, but only Zarzal and Cristal covered sufficient
area (93 % of the 1200 subplots surveyed) for the present
analysis. Both are volcanic clay soils; they differ in that
Zarzal is slightly drier than Cristal (Soil Survey Staff, 1995).
The LFPD has three slope classes: 3 – 15 %, 15– 30 % and
559
30– 60 % slope, all of which cover sufficient area to be
included. All slope categories were represented by at least
300 subplots from which 200 were randomly selected for
analysis.
Distribution of exotic versus native orchids
The relationship between distribution of O. maculata and
W. calcarata and P. stachyodes was assessed using the nonparametric Spearman’s correlation coefficient. Because many
5 5 m subplots had no plants of a given species, population
counts from two side-by-side 5 m 5 m subplots were combined, creating a 10 m 5 m plot. Subplots with no data for
either of the native species or O. maculata were omitted
because such plots contain no information regarding a potential interaction between the three species. Then 100 of the
10 m 5 m subplots were randomly selected for analyses.
R E S ULT S
Cover class and orchid distribution
Oeceoclades maculata is present in all four canopy cover
classes, but it is most abundant in cover class 3 (Fig. 1),
which is the second least disturbed cover class with an estimated forest cover in 1936 between 50 % and 80%. Here,
192, which is 56 % of the total population sampled, were
counted. Cover class 3 had a mean of 0.74 O. maculata
plants per 5 m 5 m subplot, or approx. 370 plants ha21.
Cover classes 1, 2 and 4 had far fewer orchids than cover
class 3 (Table 1; cover class 1 mean ¼ 0.18, cover class 2
mean ¼ 0.25, cover class 4 mean ¼ 0.19). The number of
O. maculata plants differed significantly among the four
cover classes (chi-square test of independence: x2 ¼ 15.96,
d.f. ¼ 3, P ¼ 0.0012; Table 1).
The frequency of plots that contained at least one orchid
plant also showed that cover class 3 was significantly preferred
over the other three cover classes (chi-square test of independence: x2 ¼ 26.3, P , 0.0001) (cover class 1 ¼ 9 %, cover
class 2 ¼ 11 %, cover class 3 ¼ 22 %, cover class 4 ¼ 11 %).
Soil type, slope of terrain and orchid distribution
Distribution of O. maculata was not associated with a
particular soil type. Average number of O. maculata plants per
5 m 5 m plot was 0.29 for Zarzal soils, and 0.27 for Cristal
soils (Kruskal–Wallis test: x2 ¼ 0.33, d.f. ¼ 1, P ¼ 0.57).
Wullschlaegelia calcarata, on the other hand, was associated
with Zarzal (Zarzal av. ¼ 0.37; Cristal av. ¼ 0.09;
Kruskal-Wallis test: x2 ¼ 9.38, d.f. ¼ 1, P ¼ 0.002), as was
P. stachyodes (Zarzal av. ¼ 0.15; Cristal av. ¼ 0.06; Kruskal–
Wallis test: x2 ¼ 7.15, d.f. ¼ 1, P ¼ 0.007).
The results for slope of the terrain were significant for all
three species. Oeceoclades maculata and P. stachyodes were
most frequent on slopes 3 – 15 % (Kruskal –Wallis tests:
O. maculata: x2 ¼ 6.27, d.f. ¼ 2, P ¼ 0.04; P. stachyodes:
x2 ¼ 13.05, d.f. ¼ 2, P ¼ 0.0001). Average number of plants
for both species was highest in this slope class (Table 2;
O. maculata mean ¼ 0.41 per 5 m 5 m subplot,
P. stachyodes mean ¼ 0.22). Distribution of the
560
Cohen & Ackerman — Land use and orchid onvasiveness
500
CC3
CC3
400
CC1
CC1
Distance (m)
300
CC2
200
CC2
CC4
100
0
0
50
100
150
200
250
300
0
50
Distance (m)
100
150
200
250
300
Distance (m)
F I G . 1. The distribution of Prescottia stachyodes (left, open triangles) and Wullschlaegelia calcarata (right, open squares) compared with that of Oeceoclades
maculata (closed circles) in the four historical cover classes of the Luquillo Forest Dynamics Plot, Puerto Rico. Small symbols represent 1– 5 individuals in a
subplot; large symbols represent .6 individuals. CC1 ¼ cover class 1, ,20 % canopy coverage in 1936; CC2 ¼ cover class 2, 20– 50 % canopy coverage;
CC3 ¼ cover class 3, 51– 80 % canopy coverage; CC4 ¼ cover class 4, .80 % canopy coverage.
TA B L E 1. The distribution of Oeceoclades maculata in the four cover classes
Number of O. maculata plants
Subplots with O. maculata
Subplots without O. maculata
Mean (s.e.) of plants per 5 5 m subplot (n ¼ 1200)
Mean (s.e.) of O. maculata per 5 5 m subplot (n ¼ 100, randomly selected)
achlorophyllous W. calcarata among slope classes was different from that of the other two terrestrial species in the LFDP
by its preference for slopes 15 – 30 % (Kruskal –Wallis: x2 ¼
6.97, d.f. ¼ 2, P ¼ 0.03), where it averaged 0.37 plants per
plot.
Class 1
Class 2
Class 3
Class 4
18
9
92
0.18 (0.08)
0.18 (0.08)
62
32
262
0.21 (0.04)
0.25 (0.09)
192
88
311
0.48 (0.06)
0.74 (0.17)
71
43
363
0.17 (0.03)
0.19 (0.07)
correlation coefficient was used to determine whether the distributions of the two native orchids were correlated with that of
O. maculata. The distributions of both W. calcarata and
P. stachyodes were negatively correlated with O. maculata
(W. calcarata and O. maculata: rs ¼ – 0.63, P , 0.0001;
P. stachyodes and O. maculata: rs ¼ – 0.43, P , 0.0001; Fig. 1).
Distribution of invasive versus native orchids
Oeceoclades maculata was more abundant than W. calcarata
in 124 of 224 of the 10 m 5 m subplots, and this was true for
P. stachyodes where 132 of 191 of the subplots contained more
O. maculata (Fig. 1). All three species had a non-normal distribution (Shapiro – Wilk test: P , 0.000), so Spearman’s rank
D IS C US S IO N
Tropical island ecosystems are at a high risk for species invasions and subsequent naturalization by non-native species.
Their high invasibility is facilitated by a combination of
heavy traffic in introductions and high levels of natural and
Cohen & Ackerman — Land use and orchid invasiveness
TA B L E 2. Results of the slope analysis for the three orchid
species tested: Oeceoclades maculata, Prescottia stachyodes and
Wullschlaegelia calcarata
Slope class
3 (3– 15 %),
n ¼ 328
subplots
Total number of
O. maculata
Subplots with
O. maculata
Mean (s.e.) for 100
random 5 5 m
subplots
Total number of
P. stachyodes
Subplots with
P. stachyodes
Mean (s.e.) for 100
random 5 5 m
subplots
Total number of
W. calcarata
Subplots with
W. calcarata
Mean (s.e.) for 100
random 5 5 m
subplots
4 (15–30 %),
n ¼ 504
subplots
5 (30–60 %),
n ¼ 368
subplots
561
invasion by O. maculata, nor were undisturbed bushland areas a
barrier to an invasive orchid, Disa bracteata, in Australia
(Bonnardeaux et al., 2007).
The first record of O. maculata in the Luquillo Mountains
dates to 1987, and in the 20 years since then this orchid has
become common in the LFDP and other parts of the
Luquillo Forest (J. D. Ackerman, unpubl. obs.). Like some
invasive herbs in other forest types, including old-growth temperate forests, time since initial colonization may be more
important than distance from human disturbance (Wiser
et al., 1998; Gilbert and Lechowicz, 2005). Although
O. maculata appears to prefer parts of the forest that have
been moderately modified by human activities, it is expected
that, over time, differences in abundance of this orchid will
diminish among the four cover classes.
135
140
68
67
83
34
0.41 (0.09)
0.26 (0.07)
0.16 (0.04)
89
54
6
38
36
6
Soil type, slope of terrain and orchid distribution
0.22 (0.06)
0.11 (0.4)
0.02 (0.01)
59
161
85
29
76
37
0.18 (0.05)
0.37 (0.08)
0.29 (0.09)
Local distribution of orchids can be affected by a number of
environmental factors, some of which may be independent of
land-use history. Intensive agriculture can severely alter soil
characteristics, and invasive species that follow abandonment
can further alter soil features (Noble et al., 2000; Flinn and
Vellend, 2005; Hawkes et al., 2005; Kulmatiski et al., 2006;
Wolfe and Klironomos, 2005). In the LFDP, farming and
logging were generally small-scale activities so damage to
the soil was not on the magnitude of large-scale farming or
clear-cut logging, nor was it widespread. Tree species composition in the LFPD was largely explained by land-use histories,
not soil types (Thompson et al., 2002).
In contrast, forest understorey herbs, including the two
native orchid species in this study, appeared to be a little
more sensitive to soil type than tree species were (Portugal
Loayza, 2005). Both native orchids preferred the drier Zarzal
soils. Soil preference of W. calcarata is most likely related
to its affinity for undisturbed locations, like cover class 4,
which was the least disturbed part of the LFDP and is
almost entirely composed of Zarzal soil (Bergman et al.,
2006). Soil preference of P. stachyodes could be due to
factors that were not part of this study such as soil pH, moisture content and, perhaps most importantly, mycorrhizal
relationships. On the other hand, the alien O. maculata
showed no preference between Zarzal and Cristal soil types,
perhaps reflecting the unusual breadth of habitat tolerance in
this species.
Analysis for an association with slope showed that
O. maculata and P. stachyodes prefer flat terrain. Both
species have shallow root systems (Ackerman, 1995), and
being in flat places decreases the chances of getting swept
away by heavy rains or landslides. This may explain the abundance of O. maculata in cover class 3, which is the flattest part
of the LFDP (Thompson et al., 2002). Wullschlaegelia calcarata, on the other hand, preferred steep locations, which is also
probably more related to its distribution and abundance in
cover class 4, the steepest part of the LFDP (Thompson
et al., 2002). Ironically, slope of the terrain acted as a
barrier and probably prevented many areas on the southern
and western ends of the LFDP from being farmed or logged
because they were simply too difficult to work (Foster et al.,
1999).
anthropogenic habitat disturbances (Foster et al., 1999; Sax
et al., 2002; Denslow, 2003; Gimeno et al., 2006). Orchids
are not often the focus of invasive species studies, regardless
of geography. From floristic works and miscellaneous literature,
it is known that Hawai’i has at least five alien species established on the Big Island, and Puerto Rico has nine (Wagner
et al., 1990; Caccia, 2005; Ackerman, 2007). Invasive orchids
and plants of other families are most commonly seen in disturbed habitats, usually those caused by human activities. The
forests where Oeceoclades maculata is abundant are in
various successional stages. Some of these recovering forests
superficially resemble old growth forests, so it is not always
obvious whether O. maculata is affected by land-use histories.
It is known that O. maculata has a broad habitat range, amply
demonstrated in Puerto Rico by its presence in lowland cactus
thorn-scrub and in broadleaf, montane rainforests. It has certainly found a suitable home in the LFDP, with a population
density of approx. 114 plants ha21. Nevertheless, plants are
not evenly distributed among the cover classes. It was shown
that O. maculata is most abundant in cover class 3, which
was the second least disturbed part of the LFDP (50–80 %
forest cover in 1936). The orchid is also scattered throughout
the three other cover classes but in densities less than half of
that for cover class 3 (Table 1).
Unaltered forest habitats are generally thought to resist establishment of invasive species (Denslow, 2003), and this seems
true for the LFDP where non-native tree species, of which
there are plenty in Puerto Rico, infrequently appear in the
forest after a hurricane but fail to persist (Thompson et al.,
2002). Invasive herbaceous herbs, however, may behave differently since the old growth forest of LFPD was not immune from
562
Cohen & Ackerman — Land use and orchid onvasiveness
Distribution of O. maculata versus native orchids
Distributions of both native orchids were negatively
correlated with O. maculata (Fig. 1). The invasive species
was more abundant than W. calcarata in 124 of 224 of the
10 5 m subplots, and the same was true of P. stachyodes
for which 132 of 191 of the subplots contained more
O. maculata (Fig. 1). This could be due to different niche
requirements or negative interactions involving their mycorrhizal symbionts. The orchids may be competing for fungal
associates or, if their associations are specific, their fungi
may compete for resources among themselves altering their
relative abundances. Oeceoclades maculata is the most abundant of the three orchid species censused in the LFDP,
which could spell trouble for the native species if it continues
to spread and competitive interactions actually do exist. These
same concerns have been expressed for Australian orchids in
face of the rapidly spreading South African species, Disa bracceata (Bonnardeaux et al., 2007).
CO NCL USI ON S
Why specific invasive species do better than others is a hotly
debated topic. They may simply out-compete native species, or
it may be a case of being in the right place at the right time
(Wiser et al., 1998; Sax et al., 2002; Denslow, 2003; Gilbert
and Lechowicz, 2005; Gimeno et al., 2006; Thuiller et al.,
2006). There is some evidence that invasive species are governed by general patterns rather than being idiosyncratic
(Arim et al., 2006). It is not clear, though, what general patterns apply to invasive orchids. All orchids have two symbiotic
interactions that may represent life-history bottlenecks: pollination and mycorrhizal fungi. One would predict that invasive
species might be autogamous, like O. maculata, or apomictic
like Zeuxine strautematica or Disa bracteata (Sun, 1997;
Bonnardeaux et al., 2007), but most may actually have
pollinator-dependent breeding systems and even low fruit production typical of most orchid populations (Ackerman, 2007;
Tremblay et al., 2005). As for mycorrhizal associations, one
may expect that invasive species specialize on a widespread
fungus, or that they exploit a broad spectrum of species.
Unfortunately, there are not yet sufficient data on these
species, but the African Disa in Australia seems to be a generalist (Bonnardeaux et al., 2007).
Regardless of what the general reasons and patterns are for
successful invasions, O. maculata has proven to be a hearty
weed that has colonized a large portion of the neotropics, and
in the LFDP all historical cover classes were invaded, including
old growth forests with minor human impacts. Where
O. maculata was most abundant, native orchids were less
common, prompting the launch of a long-term study to assess
potential negative interactions.
AC KN OW LED GEMEN T S
We thank the LFPD committee for the opportunity to work on
the ‘Big Grid’, Jill Thompson for logistical support and suggestions for the analysis part of the paper, and Jess
Zimmerman, Chris Bloch and Chris Higgins for assistance
with statistical analyses. This project was supported by
funding from NSF-Research Experience for Undergraduates
program at El Verde Field Station, University of Puerto
Rico, NSF grant number DBI-0552567, A. Ramı́rez, PI. The
LFDP has been funded by NSF grants BSR-8811902, DEB
9411973, DEB 0080538 and DEB 0218039 to the Institute
for Tropical Ecosystem Studies, University of Puerto Rico,
and to the International Institute of Tropical Forestry, USDA
Forest Service, as part of the Long-Term Ecological Research
Program in the Luquillo Experimental Forest.
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