Biological Journal ofthe Linnean Society (1993) 50: 221-233. With 11 figures
Animal-fed plants: an investigation into the
uptake of ant-derived nutrients by the fareastern epiphytic fern Lecanopteris Reinw.
(Polypodiaceae)
HONOR GAY
Department of Plant Sciences, South Parks Road, University of Oxford, England*
Received 15 April 1991, acceptedfor Publication 3 Decembcr 1992
The epiphytic fern genus Lecanopterii (Polypodiaceae) is regularly inhabited by five species of
Iridomyrmex and Crematogaster, which nest and deposit debris in the hollow rhizomes. These epiphytes
gain nutrients from ants in two ways: by rnot absorption from carton runways which surround
plants, and by uptake of solutes from ant faeces and debris through the inner rhizome walls. The
rhizome cavity surface is black, minutely pitted and bears no specialized absorptive structures.
Nutrients containing 14-glucose, 86-rubidium and 32-phosphorus injected into the rhizome cavity
were translocated through the plant. Ants inhabiting LEcanopleris were fed glycine and urea
containing 15-nitrogen, and this label was incorporated into the fern tissues. Thus ant-derived
nutrients can be incorporated into Lecanopteris tissues. The ferns may gain other benefits from the
ants such as defence against herbivores, nurture of juveniles or spore dispersal.
ADDITIONAL KEY WORDS:-Myrmeco-epiphyte
- nitrogen-I5 - nutrient uptake.
- mutualism - fern -ant - radioactive tracer
CONTENTS
Introduction . . . . . . . . . . . . . .
Nutrient transfer through the inner rhizome wall of Lecanoplnis . .
Materials and methods . . . . . . . . . .
Results . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . .
Nutrient transfer from ants to Lecanopteris . . . . . . .
Materials and methods . . . . . . . . . .
Results . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . .
The internal domatium of Lccanoplnis compared to other ant-epiphytes
The Occurrence of animals feeding plants . . . . . . .
Other benefits gained by Lccanoptcris from ants . . . . . .
Conclusions . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . .
References . . . . . . . . . . . . . .
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INTRODUCTION
Ants benefit plants which they inhabit in two ways, by feeding and/or
defending them against predators (Buckley, 1982; Huxley & Cutler, 1991).
'Present address: Church House Cottage, Scackleton, Yorkshire, YO6 4NB, U.K.
0024-4066(93/011221+ 13 $08.00/0
22 1
0
1993 The Linnean Society of London
222
H. GAY
These two roles vary with plant habit. Terrestrial, hollow-stemmed, soil-rooted
trees or shrubs are defended by their occupants: Acacia cornigera (Janzen, 1966);
Barteriajstulosa Uanzen, 1972); Leonardoxa africana (McKey, 1974), whereas nonwoody ant-inhabited epiphytes are ant-fed: Myrmecodia tuberosa (Huxley, 1976;
Rickson, 1979); Tillandsia caput-medusae (Benzing, 1970).
Epiphytes lack direct access to soil nutrients. They either obtain minerals
indirectly from the pedosphere or from sources such as the atmosphere. Nutrient
availability limits epiphyte vigour (Benzing, 1990), and a variety of nutritional
modifications such as the sterile clasping fronds of Platycerium, the nest habit of
Asplenium nidus and the domatia of ant-fed epiphytes are found within the group.
There are ten genera of ant-house epiphytes, all of which are tropical:
Myrmecodia, Hydnophytum, Anthorrhira, Squamellaria and Myrmedoma in the
Rubiaceae (Jebb, 1985; Huxley & Jebb, 1991); Lecanopteris (Gay, 1990, 1991)
and Solanopteris (Wagner, 1972) in the Polypodiaceae; Dischidia
(Asclepiadiaceae) (Weir & Kiew, 1986); Schomburgkia (Orchidaceae) (Rico-Gray
et al., 1989) and Tillandsia (Bromeliaceae) (Benzing, 1970).
Lecanopteris comprises 13 species, all of which possess hollow or expanded
rhizomes which form domatia. It is found throughout Malesia, from Queensland
to southern Thailand. The centre of diversity of the genus is Sulawesi, where
eight species, including six endemics, are found. A field survey of eight species
established that mature plants are regularly ant-inhabited, that debris and
larvae are kept in the rhizomes, and that the ants build carton runways around
the ferns (Gay, 1990; Gay & Hensen, 1992).
NUTRIENT TRANSFER THROUGH THE INNER RHIZOME WALL OF LECANOP'TERIS
Permeability of the inner wall of Lecanopteris is necessary for nutrient uptake
from ant faeces and debris in the absence of specialized absorptive structures on
the inner rhizome surface. A series of experiments was conducted using
radioisotopes to discover whether nutrients introduced into the rhizome cavity
are absorbed into the plant tissues.
Materials and methods
Three species of Lecanopteris were used: L . sinuosa (collected in Papua New
Guinea), L. pumila (Malaysia) and L. celebica (Sulawesi). In Oxford, the
specimens were planted in 'Cambark orchid grade' and kept in glasshouses at
25°C in natural daylight. After establishment, they were transferred to growing
cabinets at 25°C and 16 h illumination, for a minimum of two days before the
experiment. The specimens were mature and healthy, 20-30 cm in rhizome
length. They contained no ants during the experiment, but had been antinhabited in the field. Three radioisotopes were used (Table 1):
( 1 ) 32-phosphorus in the form of 1 pM KH,PO,, at a volume of 0.25 pl,
containing 2 pCi 32-P.
(2) 86-rubidium in the form of 1 pM RbC1, at a volume of 0.20 p1, containing
0.5 pCi 86-Rb. 86-rubidium is more stable than the isotope of potassium, and
was used as a potassium analogue in these experiments.
(3) 14-carbon in the form of 1 pM glucose, at a volume of 0.20 pl, containing
4pCi 14-C.
ANIMAL-FED PLANTS
TABLE 1.
Radioisotopes
Lecanopteris
223
injected
into
~
Radioisotope
Species
L. sinuosa
L. pumila
L. celebica
32-P
86-Rb
*
*
-
-
*
14-C
*
Y
Y
* = experiment performed
- = not performed
The radioactive solution was injected into the hollow rhizomes, using a fine
hypodermic needle. Uptake of the radioactive label was monitored with a geiger
counter immediately after injection, after 1 h, 24h and 48h. A lead shield
protected the frond readings from radioactivity in the rhizome. After 48 h, the
fronds were excised and immediately autoradiographed to avoid redistribution
of the tracer during drying. Fronds were taped to a white ceramic tile, covered
with a Mylar film, then clamped and frozen at -20°C.
Results
Immediately after injection, high levels of radioactivity were recorded in the
rhizome and none in the fronds. After 1 h, there was no radioactivity in the
fronds, and a low count was obtained after 24 h. The autoradiographs prepared
after 48 show the distribution of labelled tissue in the fronds (Figs 1-5, Table 2).
The three Lecanopteris species all showed entry of the compounds into plant
tissue. The sites of accumulation differed markedly between compounds.
Lecanopteris sinuosa concentrated the carbon ( 1 4 4 ) in the sori, but little in the
frond lamina (Fig. 1). Lecanopteris pumila and L. celebica (Fig. 2 ) showed low
absorption of 14-C. 32-phosphorus (32-P) was more evenly distributed in the
plants than 1 4 4 , but accumulated preferentially in the sori of L. sinuosa (Fig. 3).
Lecanopterispumila had no fertile fronds, but absorbed substantial amounts of 32-P
into the sterile and developing fronds. Radioactivity was also found in the solid
apex of L. pumila (Fig. 4). In contrast, rubidium accumulated preferentially in
developing rather than mature fronds of L. sinuosa (Fig. 5 ) .
TABLE
2. Relative accumulation of the radioisotopes in the organs of Lecanopteris
Organ
32-P
Frond
Sorus
Developing frond
***
0
0
86-Rb
14-C
* *
** **
*** 0
***=high radioisotope accumulation.
** =significant radioisotope accumulation
* =low radioisotope accumulation
0 =no radioisotope accumulation
224
H.GAY
Figures 1-5. Fig. 1. An autoradiograph showing concentration of 14-C glucose in the sori of a fertile
frond of I,tranopk-ris nnuosa 48 h after injection of the radioisotope into the domatium. Fig. 2. An
autoradiograph showing entry of 14-C glucose into a mature sterile frond of Lecanopleris celebica, 72 h
after in.jection of the radioisotope into the domatiurn. Fig. 3. An autoradiograph showing
concentration of 32-P in the sori of Lecanoperis sinuosu, 72 h after injection of the radioisotope into the
domatium. Xotr the presence of 32-P in the sterile frond. Fig 4.An autoradiograph showing uptake
of 32-P into a mature sterile frond and a juvenile frond of Lecanoplerispumila 48 h after injection of the
radioisotope into the domatium. Fig. 5. An autoradiograph showing uptake of 86-R into a fertile
frond, a mature sterile frond, and a juvenile frond of f,eranopferis sinuosa, 48 h after injection of the
radioisotope into thr domatium. S o t e the concentration of radioisotope in the juvenile frond.
ANIMAL-FED PLANTS
225
Discussion
The difference in the sites of accumulation of the radioisotopes may be
explained by their various biological functions. No plant parts except the sori
were visible in the 14-C glucose autoradiograph of L. sinuosa (Fig. 1). Glucose is
transported in the phloem from sources to sinks. The actively metabolizing sori
constitute a sink into which sugars are transported, and thus concentrate the
isotope. The fronds are sources of glucose, and would not be expected to
accumulate this compound. Lecanopteris pumila and L. celebica (Fig. 2) showed
little absorption of 14-C glucose. The requirement for carbon in
photosynthesizing plants would be low, with correspondingly low isotope
accumulation. Microbial and fungal activity in the rhizome may have utilized
the glucose before it could be transported into the fronds, resulting in the small
amount of labelled tissue.
Radioisotope studies on angiosperms have shown similar accumulation of 32-P
in reproductive structures (Seth & Waring, 1967). This is related to the functions
of phosphorus: as a constituent of ATP, DNA, RNA and plasma membranes
(Epstein, 1972; Marschner, 1986). The developing sori, with a high respiration
rate and proliferation of cells, have a high phosphate requirement. The presence
of phosphate in the sterile and juvenile fronds and the rhizome of L. pumila
indicates that they are also sinks for phosphates.
The distribution of 86-rubidium (86-R) in vegetative apices of Lecanopteris
complements comparable angiosperm studies. In conditions of rubidium or
potassium efficiency, this element is transported from other leaves to younger
ones, and the deficiency symptoms are manifested first in older leaves (Mengel &
Kirkby, 1987).
These experiments demonstrate that Lecanopteris species from both subgenera
can absorb nutrients across the inner rhizome wall. This suggests the likelihood
of nutrient uptake from the domatium, but does not confirm the role of ants in
any nutritional benefit.
NUTRIENT TRANSFER FROM ANTS TO LECANOPTERIS
A series of field experiments tested the hypothesis that material fed to the ants
is incorporated into the plant tissue, using heavy nitrogen, 15-N, as a tracer.
Materials and methods
Three Lecanopteris species were used: L. sinuosa and L. mirabilis (subg.
Myrmecophila), and L. pumila (subg. Lecanopteris), Isolated plants 1-5 m in length
with thriving ant colonies were selected. Field locations are shown in Table 3.
Radioactive compounds are unsuitable for use in the field; the stable nitrogen
isotope 14-N was utilized instead. Two 15-N carrier compounds were used: urea
(NH2CONH2) and glycine (NH2CH2COOH). Both compounds were 99%
15-N.
Control samples from the plants were collected before the experiment.
Samples of host tree bark were collected before and after feeding to evaluate
sample contamination with 15-N. The solution fed to the ants contained 0.1 g of
15-N compound dissolved in 3 ml 50% sucrose solution. A plastic tube of the
H. GAY
226
TABLE
3. A summary of the heavy nitrogen feeding experiments
~~
Species
Locality
Ant
Compound
No. plants
Duration
LK, PNG
BF, MAL
MM, PNG
R, PNG
GB, MAL
GBB, MAL
1.c
1.c
1.m
1.m
Urea
Glycine
Glycine
Urea
Glycine
Glycine
3
8
5
5
8
9
8 days
44days
7 days
4 days
39 days
70 days
Date
~~
L. sinuosa
L. sinuosa
L. mirabilis
L. mirabilis
L. pumila
L. pumila
c.t
C.t
Apr.
Oct.
Sep.
Aug.
Oct.
Oct.
1986
1988
1986
1986
1988
1988
KEY
LK: Lake Kutubu, Southern Highlands Province
BF: Batu Ferringhi, Penang Province
MM: Mount Mon, Milne Bay Province
R: Roguts, Western Highlands Province
GB: Gunong Berernban, Cameron Highlands
GBB: Gunong Bunga Buah, Genting Highlands
PNG: Papua New Guinea
MAL: Malaysia
1.c = Iridomynnex rordatus
1.m = I. mun'nus
C.t = Crematogartm trcubi
solution was fixed to the host tree with a tack, on or near an ant trail to facilitate
recruitment to the food source. A plastic hood was placed over the tube to
prevent splashing or dilution by rainwater. A filter paper wick was placed in the
tube to allow ants to drink without drowning.
Recruitment of workers to the solutions was rapid, and they drank avidly. The
tubes were empty on collection in all cases except experiment 6. T h e duration of
the experiment was the maximum possible (Table 3 ) . Post-experimental samples
of a solid peeled rhizome apex, a frond and adjacent host bark were collected
and dried immediately. They were analysed for 15-N enrichment by mass
spectrometry. Each sample was ground to a particle size of less than 1 mm
diameter, 4-5mg was weighed into a tinfoil tube and converted to gas by
combustion at 1000°C. Nitrogen compounds in the gas were reduced to nitrogen
by passage over copper, and total nitrogen levels were detected by capillary gas
chromatography. The gases passed into the mass spectrometer and were
separated by a magnetic field into all the isotopes of nitrogen (14-N2, 14,15-N2,
1532). The relative proportions of the gases were computed to give a percentage
of 15-N in the samples.
Results
Background levels of 15-N are accepted as 0.365% atoms (D. Clarkson p e n .
comm.), and 15-N levels in the control samples should not deviate significantly
from this figure. The results are shown by a plot of sample nature against
enrichment for each site (Figs. 6-1 1).
Lecanopteris sinuosa, experiments 1 and 2
The pre-experimental background 15-N level in the rhizomes increased four
times in experiment I (from 0.37004 to 1.257y0, Fig. 6) and five times in
experiment 2 (from 0.365% to 1.616°/0, Fig. 7). Significant post-experimental
enrichment was found in the rhizomes in experiment 1 (t2 = 7.03, P < 0.02), but
not in experiment 2 (t2 = 3.22, P > 0.05).
ANIMAL-FED PLANTS
$
2.0
y
1.8
1.6
z
J
'8
k3
I
T
1.6
1.4
1.4
1.2
1.0
1.2
1.0
0.8
0.6
0.4
Atmospheric
level
0.2
0.0
Bark
Rhizome
Sample nature
Frond
2.2 I
2.0
1.8
1.6
227
2.2
2.2
0.8
0.6
0.4
Atmospheric
level
0.2
0.0
Bark
Rhizome
Sample nature
Frond
I
1
I
T
1.4
T
1.0
0.8
0.6
0.0
1.2
1.0
0.8
c
T I
0.6
0.4
...,..
:. >,.. .
.._......
.:.:.:...
..:.:.:.:.
. . ...
Bark
Rhizome
Sample nature
0.0
Frond
2.2,
Atmospheric
level
Rhizome
Sample nature
Frond
Bark
Rhizome
Sample nature
Frond
2.2,
I
Bark
Atmospheric
level
0.2
I
Atmospheric
level
0.4
Bark
Rhizome
Sample nature
Frond
Figures 6-1 1. Levels of 15-N enrichment in samples of L. sinuosu, L. pumilu and L. mirabilis. Fig. 6.
L. sinuosa from Lake Kutubu, Papua New Guinea. Fig. 7. L. sinuosu from Penang, Malaysia. Fig. 8.
L. pumilu from Gunong Beremban, Malaysia. Fig. 9. L. pumila from Gunong Bunga Buah, Malaysia.
Fig. 10. L. mirabilis from Roguts, Papua New Guinea. Fig. 1 1 . L. mirabilis from Bonenau, Papua
New Guinea. Key:
pre-experiment,
15-N levels in L. sinuosa fronds increased from 0.367% to 1.197% (experiment
1) and 0.425% to 0.704% (experiment 2). Frond enrichment in experiment 1
was not statistically significant (t2 = 1.839, P > 0.2),but the results demonstrate
that 15-N was translocated into L. sinuosa fronds. I n experiment 2, frond
enrichment was significant (t, = 2.95, P < 0.05). Post-experimental bark
samples were not significantly enriched (t2 = 0.70; P > 0.5, t2 = 2.05, P > 0.1).
Lecanopteris pumila, experiments 3 and 4
Post-experimental rhizome samples were significantly enriched ( t 7 = 5.17,
P < 0.01; t7 = 3.49, P = 0.01). Rhizomes contained 0.84% (experiment 3, fig. 8)
zza
H.GAY
and 1.4% (experiment 4, fig. 9) of 15-N. Fronds showed greater variation in
= 16.5, P < 0.001). 15-N levels changed
enrichment ( t 7 = 2.160, P > 0.5;
from 0.366% to 0.558% in experiment 3 and from 0.366% to 1.197% in
experiment 4.Enrichment of the surrounding bark was not significant (t7= 0.85
& 0.80, P > 0.5).
Lecanopteris mirabilis, experiments 5 and 6
Anomalous results were obtained for enrichment in L. mirabilis. The bark
control samples in experiment 5 were significantly enriched, indic,ating
contamination (t4= 5.47, P < 0.01). Experiment 6 showed low levels of rhizome
enrichment (from 0.382% to 0.412y0, fig. 11). No significant increase in 15-N
levels was found for rhizomes or fronds (eg. t, = 2.37, P > 0.05).
Discussion
Levels of 15-N increased significantly in the rhizomes of L. sinuosa and
L. pumila after feeding enriched sugar to the inhabitants. There are three ways in
which 15-N could have entered the fern tissues:
(1) From ant faeces, through the inner rhizome wall.
(2) From decomposition products in debris and corpses, through the inner
rhizome wall.
(3) From 15-N on the ants’ feet, after they had stood on the 15-N-soaked wick.
The third process is not important biologically, and contamination by this
route was mimimized. The rhizome samples were solid and contained no inner
cavity surface. The epidermis was removed and the sample was washed before
analysis. Control samples of the host tree bark adjacent to the rhizome were
collected before and after the experiment to evaluate contamination;
observations suggested that the ants walked on the bark and rhizome with equal
frequency. Thus 15-N enrichment in the post-experimental bark samples would
be equivalent to that resulting from ants walking with contaminated feet within
the rhizome. Post-experimental bark was marginally but not significantly
enriched compared to background levels; a negligible amount of enrichment in
the rhizomes and fronds can be attributed to external 15-N on the ants.
The enrichment in post-experimental rhizomes and fronds of L. sinuosa and
L. pumila was considerably greater than background levels, up to 1.6% of total
nitrogen. The amount of enrichment was variable both within and between
species. The exact site and quantity of 15-N uptake was probably affected by the
locality of debris, faeces and corpses in the rhizome. Sites of 15-N accumulation
and sequestration within the fronds and rhizome are also dependent on
metabolic activity, which differs between individuals and species. Thus the
variation in levels of enrichment can be explained at two levels: variation in the
site of 15-N deposition in the rhizome, and the pattern of nitrogen metabolism of
the individual and species. The inhabitant ants, and microbial and fungal
activity in the rhizome, may also affect nutrient uptake.
The results from L. mirabilis are not significant, but the proliferation of its roots
among the debris indicates the probability of nutrient gain from ant inhabitation.
Despite the lack of specialized absorptive structures in Lecanopteris, high levels of
15-N in post-experimental in L . sinuosa and L. pumilu show that material fed to
the ants can enter fern tissues via the absorptive inner rhizome wall.
ANIMAL-FED PLANTS
229
THE INTERNAL DOMATIUM OF LECANOP'TERZS COMPARED TO OTHER ANT-EPIPHYTES
A distinction may be made between ant-house epiphytes with absorptive
structures and corresponding impermeable inner wall surfaces (Myrmecodia and
Hydnophytum); those which have aventitious roots or trichomes in the domatium
(Dischidia, Solanopteris and Tillandsia); and those which have an absorptive inner
wall surface (Lecanopteris).
The absorptive areas of the rubiaceous ant-epiphytes are confined to warts,
which are modified root tips consisting of cytoplasmic-rich cells (Meihe, 191 1;
Huxley, 1980). The cavities of Hydnophytum are little differentiated by their
absorptive capacity: their extremities are warted and pale-walled, while the
cavity centres are smooth-walled and pigmented. In Myrmecodia, tunnel-shaped
chambers are warted and the deeper shelf-like and superficial honeycombed
chambers are smooth-walled. The inhabitant ants (Iridomyrmex) keep brood in
the smooth-walled areas and place debris in the warted zones.
Huxley (1976) showed that the warty cavities of Myrmecodia could absorb
radioactivity labelled nutrients (32-P, 3543) fed to ants. Rickson (1979)
demonstrated a different absorptive pathway in Myrmecodia by feeding
radioactive compounds to Drosophila larvae. Label from the carcases placed in
the warted chambers appeared in the plant tissue.
Dischidia (Asclepiadaceae) is a scrambling epiphyte, some species of which
have highly modified leaves forming domatia. The under-surface of the leaves
has a greater number of stomata than the upper surface, which may enhance
uptake of photosynthetic gases, and is exposed to ant faeces and debris. There
are no foliar absorptive structures. Cauline adventitious roots grow into the
domatia and proliferate when the leaf cavities are moist and debris-filled,
performing the same function as the warts of the epiphytic Rubiaceae.
A similar situation occurs in Solanopteris, where the ant-house has a cauline
rather than foliar origin. Short, stout roots, densely clothed in root hairs,
originate at the tuber mouth and penetrate the domatium when it is full of debris
(Gomez, 1974). It is unknown whether the roots only grow into the tubers when
they are ant-inhabited, or whether they are a constant feature of the cavities. No
experimental work has been carried out on the absorptive capacity of domatia of
Dischidia or Solanopteris.
The bromeliads Tillandsia caput-medusae and 1.butzii have domatia consisting
of leaf base chambers containing absorptive trichomes. The trichomes can
absorb compounds such as CaC12 (Benzing, 1970).
Adventitious roots never grow into the domatium of Lecanopteris except in
L. mirabilis, although those ofother epiphytes are rarely found in the rhizome (pers.
obs.). The inner rhizome walls are not moist, nor completely smooth. They are
densely covered with minute, villi-like projections, which give the surface a
pitted appearance. These projections may be the remains of walls of the cells
which originally filled the galleries (Yapp, 1902).
The method of nutrient uptake in Lecanopteris is unique among ant-epiphytes;
it possesses no specialized absorptive structures within the domatium, nor are
debris dumps penetrated by adventitious roots. Only in the external domatium
of L. mirabilis are roots involved in nutrient uptake from debris (Walker, 1986).
The genus is also notable among vascular plants in its use of a morphologically
unspecialized internal surface for nutrient absorption.
230
H. GAY
THE OCCURRENCE OF ANIMALS FEEDING PLANTS
Myrmeco-epiphytic relationships and plant carnivory are the only two
instances where plants feed directly on animals (Thompson, 1981). Ant-house
epiphytes use debris dumps as a nutrient source; carnivorous plants dupe their
prey into approaching an apparent food source and then trap them.
Ant feeding of plants may occur in two different ways, via plant roots
anchored in an ant nest or carton, or from ant debris in a domatium. Examples
of the former abound in temperate and tropical regions. Ant-hills of British chalk
grassland have a distinctive flora confined to the granular soil of ant-hills, richer
in nutrients than the surrounding calcareous soil (King, 1977a; Woodell & King
1991).
Two distinct associations result from ant feeding of epiphytes; ant gardens and
ant-house epiphytes. The ant-garden plants benefit nutritionally (their roots
ramify through the carton), also gaining protection from herbivores and
dispersal to new ant nests (Davidson & Epstein, 1990). They have no specialized
nutrient absorption mechanisms, modifications advantageous to their ant
association are connected to propagule dispersal, such as the pearl bodies of Ficus
paraensis (Madison, 1979). Ant attractant compounds such as benziathiole are
found in the seeds of many ant-garden epiphytes, and seed analogues containing
these substances are preferentially harvested by ants (Davidson, 1988).
Facultative rooting of epiphytes in ant carton is also common (Longino, 1987).
The ant-fed epiphytes of Malesia absorb nutrients from carton and internal
debris dumps. They possess greater morphological modifications for ant-derived
nutrient uptake than ant-garden plants, but the two nutritional modes are not
distinct, since the ant-house epiphytes also root in carton.
Ant feeding of terrestrial plant domatia has not been demonstrated. Fiala et al.
( 1989) applied radio-tracers to Macaranga (Euphorbiaceae), but no label was
detected in plant tissue despite scatterings of debris in the domatium.
Animal-dispersed plants which habitually germinate in dung are also
nutritional mutualists at their germination stage. At the commensal end of this
spectrum are plants which fortuitously germinate in dung without any other
contact with the animal. Thus plants may be fed by animals as a result of
predation, mutualism or commensalism. A wide range of plant modifications
have resulted from these interactions, and facultative uptake of animal-derived
nutrients is a constant feature of the species.
OTHER BENEFITS GAINED BY LECANOPTERIS FROM ANTS
It is unlikely that the only benefit gained by Lecanopteris from the presence of
ants is nutritional. Like competition, mutualism acts diffusely rather than
specifically, both between species and in its effects on them (Hubbell & Foster,
1983). The intensity of such interactions varies in space and time (Cushmann &
Addicott, 1989, 1991). An example of a facultative association of varying
intensity is that between Caularthon bilamellatum and six species of ants. Carbon-14
tracing experiments showed seasonal changes in extra-floral use by the ants, and
varying reliance on the orchid nectar in the diet of different ant species (Fisher,
Sternberg & Price, 1990).
ANIMAL-FED PLANTS
23 1
No experimental work has been done on ant defence of Lecanopteris. Although
the inhabitants are small and non-stinging (Iridomyrmex Mayr and Crematogaster
Lund.), the presence of an ant colony in a plant is likely to deter some predators.
Activities beneficial to hollow epiphytes such as defence are the natural reaction
of ants towards a threat to their nest. Benefits accruing to young plants with solid
stems cannot be thus interpreted. Juvenile plants commonly grow near
established Lecanopteris, are connected to them by carton runway, and the
rhizome and roots are semi-buried in carton. Ant protection is most valuable at
the establishment stage of angiosperms (O’Dowd, 1979; Schupp, 1986).
Predation at the juvenile stage can be a major factor influencing mortality of the
entire plant, in contrast to its decreased effect on mature individuals. This is
analogous to the greater value of ant protection of developing seeds, leaves and
shoots, before chemical defences are developed. Juvenile Lecanopteris seen were
scarcely affected by herbivory, although Jermy & Walker (1975) reported that
cultivated sporelings of L. mirabilis were devastated by slugs, indicating that ant
defence of juveniles may occur.
Young, solid Lecanopteris cannot absorb ant-derived nutrients internally.
However, their partial burial in carton indicates that they may gain minerals
from root absorption prior to development of a hollow rhizome. Protection of
young, vulnerable stages may be the greatest benefit gained by Lecanopteris.
Mature plants can survive without ants (Gay, 1990; Gay & Hensen, 1992), but
ant activities may significantly affect survival and vigour of juveniles.
Holttum (1954b) and Janzen (1974) have suggested that ants disperse the
spores of Lecanopteris, eating the oil-rich bodies observed on the spores of
L. sinuosa. I have never seen ants harvesting the sori during the day or dusk, but
have no data a t night, when Janzen reported ant dispersal. During the day, all
regular inhabitants of Lecanopteris forage over the entire plant, perhaps
incidentally dispersing the spores.
The spores of L. mirabilis bear long filaments (Karsten, 1895). Tryon (1985)
interpreted structures as adaptations for ant dispersal. Walker (1985) presented
an alternative explanation implicating the avoidance of intra-gametophytic
selfing by dispersal of the 16 spores in a sporangium as a filament-bound unit.
There are no supporting data for either hypothesis.
CONCLUSIONS
The absorptive nature of the inner domatium wall and the pathway of
nutrients from ants to Lecanopteris have been demonstrated. The regular presence
of debris dumps and faeces in the domatium provides a continuous source of
nutrients, although the extent of its utilization by Lecanopteris has not been
established.
Benefits accruing to Lecanopteris as a result of its ant association may be a
combination of feeding, defence, nurture of juveniles or dispersal. The ant
interaction may not affect survival of strong individuals, but may be critical for
less healthy ones, and especially for immature plants. The variety of benefits
which may be gained by Lecanopteris, and the range of intensity with which the
association may affect different individuals emphasize that mutualisms cannot
be defined in single-effect terms.
232
H. GAY
ACKNOWLEDGEMENTS
I would like to thank my D. Phil. supervisor, Dr Camilla Huxley, for critically
reading the manuscript. The field studies were carried out whilst I was working
at the University of Lae, Papua New Guinea and the Forest Research Institute
of Malaysia, and I thank Mr Bob Johns and Dr Francis Ng for placing their
extensive facilities at my disposal. Dr Brian Loughman assisted with radioactive
techniques and Dr David Clarkson analysed samples by mass spectrometry at
Long Ashton Research Station. Fenella Parrott was a valuable field assistant and
gave statistical advice in the preparation of this manuscript. My D. Phil. and the
fieldwork in Papua New Guinea were funded by the Claridge Druce Memorial
Scholarship in Plant Taxonomy, and the fieldwork in Malaysia by the
Leverhulme Trust.
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