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Insectes soc. 47 (2000) 313– 316
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Insectes Sociaux
Research article
Ant nests in tank bromeliads – an example of non-specific interaction
Nico Blüthgen 1, M. Verhaagh 2, W. Goitía 3 and Nils Blüthgen 4
1
2
3
4
Botanisches Institut der Universität Bonn, Meckenheimer Allee 170, D-53115 Bonn, Germany
Current address: Rainforest CRC, P. O. Box 6811, Cairns, Qld 4870, Australia, e-mail: [email protected]
Staatliches Museum für Naturkunde, Erbprinzenstrasse 13, D-76133 Karlsruhe, Germany, e-mail: [email protected]
Universidad Simón Rodríguez, Apartado 47925, Caracas 1010, Venezuela, e-mail: [email protected]
Theoretische Biologie, Humboldt Universität, Invalidenstrasse 43, D-10115 Berlin, e-mail: [email protected]
Received 2 September 1999; revised 20 April 2000; accepted 10 May 2000.
Summary. Four species of epiphytic tank bromeliads on an
island in the Orinoco river in Venezuelan Amazonia were
inhabited by 13 ant species from four subfamilies. None of
these ant species are known as specialised plant-ants. A Monte
Carlo randomisation test showed that ants were randomly
distributed among host plants: (1) there was no association
between particular ant species and bromeliad species, and (2)
there was no vertical stratification of the ant community between bromeliads sampled on the ground and at two height
classes in trees. This contrasts with the few published data
on the distribution of ants on terrestrial myrmecophytes and
epiphytes, respectively, to which we applied the same analytical method.
liads are often inhabited by ant colonies (Schimper, 1888;
Bequaert, 1922; Wheeler, 1942; Dejean et al., 1995), especially intermediate types with characteristics of both phytotelm
and myrmecophytic bromeliads (e.g., Aechmea bracteata:
Dejean and Olmsted, 1997). In such unspecific hosts,
ant-inhabitants can be expected to be unspecific as well
(Skwarra, 1934; Davidson and McKey, 1993). In four species
of tank bromeliads of the lowland Amazonian rainforest corresponding to the “variable tank type” in Dejean et al. (1995),
we examined whether ant inhabitants were randomly distributed or structured, using randomisation tests, and if ant taxa
could be considered opportunistic or specialised. We use our
study to recalculate and discuss other reported ant-plant
matrices by applying the same statistical methods.
Key words: Formicidae, Bromeliaceae, Monte Carlo methods,
randomisation, commensalism.
Materials and methods
Introduction
Myrmecophytes – plants offering highly modified structures
that provide nesting space for ants – are widespread in tropical lowland rainforests and often regarded as classical example of co-evolution (Janzen, 1966; Davidson and McKey,
1993; Jolivet, 1996). Ant-inhabitants of myrmecophytes were
found to be relatively host-specific at least on a local scale
(Fonseca and Ganade, 1996). In less co-evolved systems,
however, one would expect a relatively low degree of specificity between partners (Jordano, 1987).
Bromeliads include a few “myrmecophytic” species
with morphological modifications, but more commonly
“non-myrmecophytic” species such as typical tank bromeliads (phytotelm types) (Benzing, 1970, 1990; Huxley, 1980;
Davidson and Epstein, 1989). Nevertheless, tank brome-
The study area is located on an island in the upper Orinoco river near
La Esmeralda, Venezuela, two km south of the Surumoni crane plot
(3°8¢ N and 65°38¢ W). Parts of the island and study area were seasonally flooded. Mean annual rainfall is 2000 mm (Szarzynski and Anhuf,
in press). Our study took place between June and August 1998 during
the wet season.
In the wide regions of the terra firme rainforest that had been
studied in the surrounding, the population density of bromeliads and
other epiphytes is relatively low (Engwald et al., 2000), which seems
typical for lowland Amazonian rainforests (Grubb et al., 1963). In our
study site, however, trees were bearing a conspicuously high density of
epiphytes, possibly due to the moist conditions on the island. This
situation enabled us to examine 77 bromeliads from four species, all
sampled within an area of approximately 0.1 ¥ 1 km along the river bench
of the Orinoco. (This area contained a considerably higher density of
bromeliads, but many of them were not accessible to us). The species
were Guzmania lingulata, Tillandsia adpressiflora, Vriesea procera,
and V. rubra (Bromeliaceae: Tillandsioideae). We sampled bromeliads
that were fallen on the ground (17 plants, most commonly large plants
of V. procera that survived and sometimes flowered on the ground) as
314
N. Blüthgen et al.
Ants in bromeliads
well as epiphytes from 23 trees or shrubs that were partly accessed with
the aid of the single-rope technique. For each bromeliad, size parameters were recorded (number, length and width of leaves, height and
width of the rosette). All leaf bases were checked for ant nests, and ant
colony size was roughly estimated. Ants were recorded only when
eggs or larvae were observed, collected in alcohol and deposited in the
National Museum in Maracay (Venezuela) and Natural History Museum in Karlsruhe (Germany).
For analysing the level of species sorting (compartmentalisation) of
the ant-plant matrix, we used a randomization method that is directly
comparable with the study by Fonseca and Ganade (1996) on terrestrial
myrmecophytes (chi-square statistics were not permitted, since most
expected cell entries were too low, see Fowler and Cohen, 1996). For
this analysis, 25000 random matrices were generated with the same row
and column totals as in the empirical matrix (computer program based
on the algorithm from Patefield, 1981). For each matrix with r rows and
c columns, the test statistics,
T = ∑ (a r, c · log a r, c )
was obtained, including all cell entries ar, c (the equation is derived from
log-likelihood statistics). Highly structured matrices (implying a high
degree of compartmentalisation between species, see Fonseca and
Ganade, 1996) result in higher values of T as random matrices, while
overdispersed matrices yield the lowest T. We compared the statistics of
our empirical data (Tobs) with the distribution of the statistics of all generated random matrices (Tran). The significance level p of the difference
between Tobs and the random sample was calculated as
p = min (PL , PU ),
where PL is the proportion of all Tran being equal or smaller than Tobs , and
PU is the proportion of all Tran being equal or higher than Tobs (Manly,
1997). (The computer program is available from Nils Blüthgen or under
http://itb.biologie.hu-berlin.de/~nils/stat/).
Results
Of 77 individual bromeliads studied here, 43 (56%) were
lacking ant nests. In 25 bromeliads, we found nests of a single
ant species, while in seven cases two ant species co-occurred
in different regions of the same bromeliad, and three versus
four different ant species in one plant were found a single
time each, respectively. Ant-free bromeliads were found in
all four species, but occurred most frequently in Tillandsia
adpressiflora (in 24 of 34 individuals).
Overall, 13 ant species were nesting in the plants (Table 1).
They belonged to eight genera from four subfamilies:
Cyphomyrmex, Pheidole, and Wasmannia (Myrmicinae),
Dolichoderus (Dolichoderinae), Paratrechina (Formicinae),
Pachycondyla, Platythyrea, and Odontomachus (Ponerinae).
All frequent ant species (> 2 nests) occurred in at least
two different bromeliad species. In some cases, ant species
were found to occupy two or three bromeliads on a single tree
or within a small area on the ground. This might be due to
multiple nests of a single colony and cannot be considered
independent; thus replicates within the same area were excluded from statistical analyses of the matrix (see legend in
Table 1). More commonly, however, ant inhabitants varied
when epiphytes were sampled from the same tree.
Ant species were not compartmentalised between bromeliad species. The test statistics (Tobs.) of the ant-by-plant
matrix (Table 1a, without numbers in brackets) was 26.8 and
was similar to the statistics obtained by random simulations
(mean Tran.= 25.4, ± 2.6 S.D.). 29% of all values for Tran were
above or equal to Tobs and 71% below or equal to Tobs , hence
the observed matrix was not significantly different from random matrices (p = 0.29). Furthermore, the ant community
was not significantly structured between epiphytes on the
ground or two height classes in trees. The statistics of the
ant-by-height matrix (Table 1b) did not differ significantly
from random matrices (Tobs = 26.7; Tran = 24.0, ± 2.3; p = 0.12).
Ant colony sizes ranged from 50 to 200 ants, as in most
species, to approximately 1000 ants (Pheidole sp. G). There
were weak, but significant positive correlations between ant
colony size and certain size parameters of the bromeliads
(Spearman’s rank correlation between colony size and
Table 1. Ant nests (a) in four bromeliad species, and (b) in different height levels above ground. Numbers are given for the occurrence of interactions
on different trees or regions on the ground. If interactions were repeated on the same tree or ground site, the total of recorded interactions is shown in
brackets. In cases marked with *), two different epiphyte species occurred in close proximity and were not considered independent in (b), so that the
total in (a) is higher than in (b). Reproductive ants (alates) occurred in ant species marked with R).
Ant species
Cyphomyrmex minutus R)
Cyphomyrmex rimosus
Dolichoderus laminatus R)
Pachycondyla villosa
Paratrechina sp. A
Paratrechina sp. C R)
Pheidole sp. D R)
Pheidole sp. E
Pheidole sp. F R)
Pheidole sp. G
Platythyrea angusta
Odontomachus haematodus R)
Wasmannia auropunctata
(a) Bromeliad species
(b) Height above ground
Guzmania
lingulata
Tillandsia
adpress.
Vriesea
procera
Vriesea
rubra
on ground
1–4 m
5 – 18 m
–
–
–
–
–
2
3
–
–
–
–
–
–
3 *)
–
–
–
1
–
3 *)*)
2 *)
–
–
–
1 *)
1 (2)
2 *) (3)
2
–
–
–
1
5 *) (7)
1
–
–
–
3
–
–
–
1
1
–
1
1 *) (2)
1
1 (2)
1 (2)
1
1 *)
–
3 (4)
1
–
–
1
–
3 (5)
2 (3)
1 (2)
–
–
3 (4)
–
–
1
–
–
–
3
6 (8)
1
–
–
–
1
–
1 (2)
–
1
1
–
1
2
–
–
1 (2)
1
–
1 (2)
Insectes soc.
Vol. 47, 2000
number of leaves (r = 0.41), or colony size and plant height
(r = 0.43; p < 0.05).
Some ant nests were found in relatively dry conditions
between the outer leaves, others occurred in wet parts of the
leaf rosette. Reproductive alates were found in colonies of six
ant species during the study (Table 1).
Discussion
In tank bromeliads as a model for non-specific host plants,
ant inhabitants were found to be non-specific as well and
probably highly opportunistic in respect to host plant species
and height above ground. Among the ant species or genera
recorded here, there are no obligate or common inhabitants
of myrmecophytes (Benson, 1985; Davidson and Epstein,
1993; some uncertainty remains for morphospecies of Pheidole). The two small species of fungus growing Cyphomyrmex (tribe Attini) are known to nest in soil or rotten wood
on the ground as well as in suitable arboreal substrates like
epiphytes or epiphytic humus. The very common Wasmannia
auropunctata is an opportunistic coloniser of a broad scale of
natural cavities including litter, dead wood, bark, epiphytes
etc. throughout the whole vertical height range. Most Paratrechina and Pheidole species in the neotropics nest in the
soil or in rotten wood on the ground, but nests of different
species have also been found in the lower vegetation and in
tree crowns including epiphytes. It is unclear if the encountered species are true arboreal ones. A ground dwelling species
is Odontomachus haematodus nesting in the soil or between
plant material near the ground while nests of Platythyrea
angusta are most commonly found in rotten wood or cavities
in living or dead trees. The only known true arboreal species
in our survey are Dolichoderus laminatus and Pachycondyla
villosa, neither known as obligate epiphyte inhabitant, although at least the latter is often found nesting in certain
epiphytes (Brown, 1975; Dejean and Corbara, 1990; MacKay, 1993; Dejean et al., 1995; Verhaagh, unpubl. data).
All ant genera and many of the ant species recorded in our
study, overlap with other reports of ant faunas in bromeliads
(Skwarra, 1934; Wheeler, 1942; Dejean et al., 1995; Dejean
and Olmsted, 1997). Furthermore, co-inhabitation of two or
more ant nests within a single plant was frequent, also reported by other authors (Skwarra, 1934; Dejean et al., 1995;
Dejean and Olmsted, 1997).
The inclusion of both tree- and ground-dwelling ants
indicates that bromeliads might function as refuges for
partially flooded terrestrial habitats as in the study area here.
We found no statistical evidence for stratification between
ant species in bromeliads of different height levels (unlike
Brühl et al., 1998; Longino and Natkarni, 1990 for other ant
faunas).
The only quantitative community analysis covering
various myrmecophytes so far, was carried out by Fonseca
and Ganade (1996) who focused on terrestrial myrmecophytes in the Amazonian rainforest near Manaus. Their
ant-plant species matrix was shown to be significantly structured. Data by Cabrera and Jaffé (1994) in Venezuelan rain-
Research article
315
forests lead to the same conclusion that terrestrial myrmecophytes were compartmentalised: when the same randomisation test is applied to their data, the statistics of the observed
matrix is significantly larger than the statistics of the random
matrices (Tobs = 242.9; Tran = 206.8 ± 4.0; p < 0.001). In a
study of bromeliads from a low inundated forest in Mexico
by Dejean et al. (1995), three Tillandsia species can be a
posteriori classified as “myrmecophytic” or “myrmecophytic-like” (> 50% of individual bromeliads inhabited by ants),
and four species as “variable tank type” (< 40% inhabited).
Recalculation of their matrix and application of the same
statistics as above shows that ant inhabitants in myrmecophytic-like and myrmecophytic bromeliads are highly structured (Tobs = 259.0; Tran = 197.5 ± 4.8; p < 0.001). Bromeliads
of “variable tank type” can also be considered structured, although to a lesser extent (Tobs =17.2; Tran =13.1 ± 2.0; p = 0.04).
These species – in contrast to the “variable tank” bromeliads
in our study – may exhibit a greater interspecific variation of
microhabitat conditions that could account for the species
sorting of ants.
In conclusion, all studies of myrmecophytic plants
showed a structured ant community in contrast to our findings
of a random structure in non-myrmecophytic plants. However, none of the cited studies treated the problem of overlapping ant colonies in neighbouring plants (leading to
pseudoreplicates in the ant-plant matrix), hence the degree of
compartmentalisation might be overestimated. To evaluate, if
the degree of species sorting could be a result of specialisation in ants and/or plants, more quantitative community
studies are needed, particularly about commensalistic, nonspecific ant-plant systems.
Acknowledgments
Thanks are due to Deutsche Forschungsgemeinschaft (DFG) (Ba 605/
6-2) and Studienstiftung des deutschen Volkes for financial support, to
the Ministerio del Ambiente y de los Recursos Naturales Renovales in
Venezuela (MARHR and SADA) and the Austrian Academy of Science
for logistical support of the project, to Silke Engels and Arnhild Althof
for field assistance, and to an anonymous referee for valuable comments
on the statistics used.
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