Ant-houses in the fern genus Lecanopteris Reinw. (Polypodiaceae): the rhizome morphology and architecture of L. sarcopus Teijsm. & Binnend. and L. darnaedii Hennipman

The rhizome morphology and architecture of L. sarcopus Teijsm. & Binnend. and L. darnaedii Hennipman. The rhizomes of the epiphytic fern Lecanopteris are highly modified and shelter ants, either in cavities or between the rhizome underside and the host tree. Different emphases on the relative contributions of morphology and architecture to the form of the ant-house exist in the genus, and are illustrated by a discussion of the rhizomes of L. sarcopus and L. darnaedii from Sulawesi, Indonesia. Lecanopteris sarcopus has dimorphic rhizomes, differentiated into solid, frond-bearing sections and hollow, frondless, ramifying ant-house branches. The internal morphology is simple; complexity in the rhizome structure is the result of profuse growth and branching of the ant-house branches. The rhizome of L. darnaedii is internally differentiated into two gallery and chamber systems, arranged vertically, with one directly above the other and running the length of the rhizome. Lecanopteris darnaedii does not branch profusely; 90–100% of primary side shoots develop but do not commonly grow beyond four to five internodes. Thus, in L. darnaedii plant architecture is restrained but morphology is intricate, while the reverse is true for L. sarcopus. Both species are equally regularly inhabited by ants.     

Ant specificity and behaviour in mutualisms with epiphytes: the case of Lecanopteris (Polypodiaceae)

Seven species of the fern Lecanopteris: L. sinuosa, L. sarcopus, L. mirabilis, L. curtisii, L. pumila, L. celebica and L. damaedii are regularly inhabited by ants of five species: Iridomyrmex cordatus, I. murinus, Crematogaster treubi, C. difformis and Camponotus pallidas. Inhabitation is not obligate; either party can survive without the other, but ferns without ants are rare in their natural habitat. The total recorded diversity of ants in Lecanopteris is 31 species, 20 of which were only recorded once.
All five regularly inhabiting ant species kept larvae in the domatium (82% of Lecanopteris specimens examined). The major ant species inhabiting Lecanopteris deposited debris in the domatium, segregated from their brood (90% of Lecanopteris specimens). Iridomyrmex murinus did not build carton around the rhizomes, but the other major inhabitants constructed runways in 79% of Lecanopteris specimens. Goccid cultivation was variable within ant and plant species: I murinus tended them in 50% of specimens, and homopterans were also recorded with Crematogaster treubi (39%), C. bomeensis (27%) and I cordatus (16%). A high frequency of ant colonies inhabiting Lecanopteris , keeping larvae, depositing debris, building carton runways, and occasionally keeping coccids has been established. Specificity of ant species is high within a population of Lecanopteris , or a given habitat or geographical area, but outside the ranges of regular inhabitants other ant occupants are found. Comparable data from other genera of ant-epiphytes with domatia show similar diversity of inhabitance over geographical areas; no data are available within single plant populations.     

Rhizome structure and evolution in the ant-associated epiphytic fern Lecanopteris Reinw. (Polypodiaceae)

GAY, H., 1993. Rhizome structure and evolution in the ant-associated epiphytic fern Lecanopteris Reinw. (Polypodiaceae). The Lecanopteris rhizome is expanded or hollow, and is used as a nest by ants of the genera Iridomyrmex and Crematogaster. The 13 species of Lecanopteris display six rhizome forms, unequally distributed between two subgenera. Subgenus Myrmecopteris comprises four species, each possessing a characteristic rhizome: L. mirabilis has a solid, arched rhizome, with the domatium between the rhizome underside and host trunk; L. sarcopus displays dimorphism between solid frond-bearing axes and hollow, frondless side branches; the rhizome of L. Crustacea is hollow but phyllopodia are solid; L. sinuosa has hollow rhizomes and phyllopodia. The architecture of L. mirabilis, L. sarcopus and L. Crustacea results in a compact, many-layered domatium, but L. sinuosa has a tittle-branched habit. Members of subg. Lecanopteris are completely hollow and have a compact architecture: six species typified by L. pumila have a central gallery and hollow phyllopodia, and three species typified by L. darnaedii have two gallery and chamber systems. The genus Lecanopteris is unlikely to be monophyletic; its nearest relative is Phymalodes. Phylogeny in subg. Myrmecopteris is unclear; no gradation of rhizome complexity exists. In subg. Lecanopteris, L. curtisii is considered most similar to the ancestral species, giving rise to the L. pumila group, which engendered the L. darnaedii group.     

In vitro studies on apogamy, apospory and controlled differentiation of rhizome segments of the fern, Ampelopteris prolifera (Retz.) Copel.

Apogamy was induced in the fern Ampelopteris prolifera by culturing the gametophytes on mineral nutrients supplemented with various concentrations of sucrose. Higher concentrations (5–8%) of sucrose were detrimental to prothallial growth, while in lower concentrations (2–3 %) apogamy was delayed. Gametophytic callus was induced from the germinating spores by culturing them on 2,4-D rich (3–5 mg/1) media. The differentiation of this gametophytic callus was conditioned by sucrose and auxin concentrations of the medium. In the presence of sucrose, calli responded like prothalli, while in the presence of 2,4-D, differentiation was delayed or completely inhibited. Apospory was induced on the sexual cotyledonary and juvenile sporeling leaveS. Leaves with petiole, excised from aseptically raised plants from excised cultured buds, also exhibited apospory, while no success was achieved with the excised leaves of the parent plantS. Rhizome segments of various length were cultured on media containing different concentrations of sucrose. The differentiation of rhizome segments into gametophytes or sporophytes was conditioned by the length of the rhizome segments and the sucrose concentration of the medium. The possible significance of all the results is discussed.     

Immunocytochemical localization of cytokinin in Azolla filiculoides

Abstract

In the small aquatic fern Azolla filiculoides, cytokinin immunolocalization was performed in longitudinal axial sections of plantlet shoots. The reaction was detected: (i) in the contiguous cell sheet which encircles vascular tissues, (ii) in shoot and root meristem target cells, and (iii) in the teat cells of the leaf cavity pore. Our results demonstrate, for the first time, that in ferns the cytokinin translocation pattern can be different to that described in seed plants. Thus, this class of hormones is translocated, via vascular tissues in seed plants, whereas in Azolla it depends upon a sheet layer of cells encircling the conducting tissues. In shoot and root meristems, cytokinin distribution widely differs; in fact, in the shoot apex, the signal is present only in a few target cells, whereas in the root the signal is localized in numerous contiguous cells. Another finding concerns the clear signal observed at the level of the teat cells delimiting the pore which connect the leaf cavity with the exterior. This result provides indication that cytokinins, which are known to be involved also in light perception, might play a key role in the control of Anabaena movement into and out of the leaf cavity. This is the first report concerning cytokinin distribution in fern cells and tissues. Our results suggest that these hormones are implicated in the different plant organs in very different and specific functions.     

Reviews of publications

The Paleobiology of Trace Fossils, edited by Donovan, S. K. John Wiley & Sons
Biological Systematics. The State of the Art, by A. Minelli.
The Portable Darwin, by Porter, D. M. and Graham, P. W. Penguin
Ecological Understanding. The Nature of Theory and the Theory of Mature, by Pickett, S. T. A., Kolasa, J. and Jones
Community Ecology, by R. J. Putman.
Volcanism and Early Terrestrial Biotas. Eds Rofle, Clarkson and Panchen.
Burr FA, Evert RF. 1982. A cytochemical study of the wound-healing proteins in Bryopsis hypnoides.
Gould SJ. 1989. Wonderful life: the Burgess Shale and the nature of history.
Dow MM, Cheverud JM, Rhoads J, Friedlaender J. 1987b. Statistical comparison of biological and cultural/history variation.
Gay HJ. 1990. The ant association and structural rhizome modifications of the far eastern fern genus Lecanopteris (Polypodiacaea).     

Ants impact sawfly oviposition on bracken fern in southern California

Although it has been speculated that ant visits to extrafloral nectaries of bracken fern may convey a fitness benefit for the plant, this has never been demonstrated with native herbivores and natural insect densities. We tested the hypothesis that ants attracted to extrafloral nectaries of bracken fern provide a mutualistic benefit by protecting fronds from herbivore damage in a field manipulation experiment in southern California. We examined densities of sawfly eggs and larvae on bracken fronds with and without ant exclusion. Because bracken fern in this region is also impacted by nitrogenous air pollution, we included an N addition treatment. We found that sawfly egg abundance was significantly higher for fern plants when ants were excluded, regardless of N treatment. Ants tended to have higher abundance on fertilized plants, but there was no interaction between N additions and ant exclusion. Bracken fern may derive a fitness benefit from attracting ants during the early phases of plant growth, through decreased herbivore oviposition, rather than through the deterrence of feeding larvae.     

Uptake of ant-derived nitrogen in the myrmecophytic orchid Caularthron bilamellatum

Background and Aims Mutualistic ant-plant associations are common in a variety of plant families. Some myrmecophytic plants, such as the epiphytic orchid Caularthron bilamellatum, actively form hollow structures that provide nesting space for ants (myrmecodomatia), despite a substantial loss of water-storage tissue. This study aimed at assessing the ability of the orchid to take up nitrogen from ant-inhabited domatia as possible trade-off for the sacrifice of potential water storage capacity. Methods Nitrogen uptake capabilities and uptake kinetics of (15)N-labelled compounds (NH(4)(+), urea and l -glutamine) were studied in field-grown Caularthron bilamellatum plants in a tropical moist forest in Panama. Plants were either labelled directly, by injecting substrates into the hollow pseudobulbs or indirectly, by labelling of the associated ants in situ. Key Results Caularthron bilamellatum plants were able to take up all tested inorganic and organic nitrogen forms through the inner surface of the pseudobulbs. Uptake of NH(4)(+) and glutamine followed Michaelis-Menten kinetics, but urea uptake was not saturable up to 2 mm. (15)N-labelled compounds were rapidly translocated and incorporated into vegetative and reproductive structures. By labelling ants with (15)N in situ, we were able to prove that ants transfer N to the plants under field conditions. Conclusions Based on (15)N labelling experiments we were able to demonstrate, for the first time, that a myrmecophytic orchid is capable of actively acquiring different forms of nitrogen from its domatia and that nutrient flux from ants to plants does indeed occur under natural conditions. This suggests that beyond anti-herbivore protection host plants benefit from ants by taking up nitrogen derived from ant debris.     

A reassessment of the relations in Malaysia between ants (Crematogaster) on trees (Leptospermum and Dacrydium) and epiphytes of the genus Dischidia (Asclepiadaceae) including 'ant-plants'

Three species of epiphytic Dischidia have been investigated in terms of their relationship to ants on trees. Two species, D. parvifolia and D. astephana , are associated with ants and trees in montane areas. A clear association has been found between ants of the genus Crematogaster and the tree Leptospermum flavescens. This relationship is complex and probably both organisms benefit from the association. The ants live in tunnels in the wood of the major branches and the trunk, and the entire tree is occupied by one ant colony. Trees occupied by ants are maintained by the ants substantially clear of epiphytes other than the two species of Dischidia. The potential benefits to the tree and to the ants of this association are noted. The roots of D. astephana and D. parvifolia penetrate into the cavities of these ant nests and presumably gain nutrients from waste in the ant nests. Both Dischidia species are effectively scavenging upon the waste material from the ant-tree association. The leathery dome-shaped leaves of D. astephana are not vital to the development of the scavenging habit as D. parvifolia has lens-shaped leaves, but may offer some advantage to D. astephana by the uptake of nutrients from waste deposited by the ants under the dome-shaped leaves by interception of stem flow and by uptake of gaseous waste. Ants do not nest under these leaves. Seeds of these species of Dischidia are taken by ants into the central woody area of the ant nest where they germinate. Both Leptospermum and Dischidia can be visualized as showing adaptations to a nutient-deficient tropical montane environment. These adaptations are discussed as is the need for reassessment in this genus of the term 'ant-plant', and the need for wider recognition of the 1ant-tree' relationship between Crematogaster and Leptospermum.     

Anatomy of six species of Dryopteris ferns (Dryopteridaceae) from Mexico

Rhizome and foliar anatomy of the Mexican Dryopteris Adans. species were studied and compared with other Dryopteridaceae and other fern families to identify anatomical features with diagnostic value. The anatomy of rhizome, stipe, and blade is similar in species of the Dryopteris patula complex. The cells with un-lignified, thickened wall, with cap or U-shape around the meristeles belong to the collenchyma, in contrast with other fern families. Dryopteris wallichiana (Spreng.) Hyl. is anatomically distinguished from the other studied species by having more layers of sclerenchyma and meristeles on the stipe, and by the lack of sclereid nests on the rhizome. Dryopteris rossii C. Chr. and D. maxonii Underw. & C. Chr. are characterized by the presence of crystals on the periphery of rhizome nests. D. maxonni and D. wallichiana lack blade glands.     

Ants inhabiting myrmecophytic ferns regulate the distribution of lianas on emergent trees in a Bornean tropical rainforest

Little is known about the spatial distribution of lianas on emergent trees in tropical rainforests and the factors affecting this distribution. The present study investigated the effects of an arboreal ant species, Crematogaster difformis, which forms myrmecophytic symbioses with two epiphytic ferns, Lecanopteris sp. and Platycerium sp., on the spatial distribution of lianas associated with emergent trees. Living lianas were placed onto trunk surfaces inside and outside the territories of the ants in the canopy, to examine their ability to remove them. The number of leaves pruned by the ants was significantly higher on lianas inside than outside their territories. The spatial overlap of the distributions of lianas and the two ferns on emergent trees were then examined. The frequency of liana colonization of tree crowns was found to be significantly lower on trees with than without ferns. Under the natural conditions, C. difformis workers were observed biting and pruning the lianas. These results suggest that C. difformis regulates the distribution of lianas on emergent trees.     

Ant-fed plants: comparison between three geophytic myrmecophytes

In their association with myrmecophytes (i.e. plants that shelter a limited number of ant species in hollow structures), ants sometimes provide only poor biotic protection for their host plants, but may supply them with nutrients (myrmecotrophy). We studied three geophytic myrmecophytes growing in the understorey of Guianian rain forests. Allomerus ants build spongy-looking galleries rich in detritus and insect debris over the stems of their host plants [ Cordia nodosa Lamark (Boraginaceae) and Hirtella physophora Martius & Zuccharini (Chrysobalanaceae)], while Pheidole minutula Mayr colonies deposit their waste in the leaf pouches of their host plant [ Maieta guianensis Aublet (Melastomataceae)]. This waste is more nitrogen-rich than that found in the Allomerus galleries, themselves containing more nitrogen than the plant leaves. Using stable isotope analysis we noted a significant difference in δ¹⁵N between ant-occupied and unoccupied plants only for Maieta , for which 80% of the host plant nitrogen is derived from Pheidole waste. Experiments on all three plants using a ¹⁵N-supplemented solution of NH₄Cl confirmed these results, with an increase in this isotope noted between control and experimental plants only for Maieta . The internal surfaces of Maieta leaf pouches bear protuberances whose likely role is to absorb nutrients from the Pheidole waste. The alternative hypothesis, that these protuberances play a role in provisioning ants, was rejected after comparing their structure with those of extrafloral nectaries and food bodies in a histological study.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 433–439.     

Vascular Organization and some Aspects of the Morphology of the Rhizome of Gymnogrammitis dareiformis

Gymnogrammitis dareiformis, the taxonomically controversialdavalliaceous fern has a parenchymatous rhizome, in the groundtissue of which groups of 1–16 thick-walled cells (withpeg-like protrusions on inner walls) are irregularly scattered.Paleae clothing the rhizome are basally attached, gland-tippedand bearing unicellular marginal hairs. The vascular cylinderis a radially-symmetric dictyostele dissected by spirally-arrangedleaf gaps into slender reticulated meristeles. Some of the dorso-laterallyplaced leaves alone are fully developed; most other leaves aresuppressed and some are highly reduced (the larger reduced leavesappear as protrusions on the rhizome and have a well-formedleaf base). The leaf trace of developed as well as the largerreduced leaves is a channel-shaped loose reticulum of four vascularstrands; the trace of the reduced leaves is smaller and endsblindly at the leaf base. The leaf trace of the smaller reducedleaves is vestigial and represented often by only a pair ofvascular strands fusing into one and ending blindly in the cortexof the rhizome. The leaf trace of suppressed leaves fuses backwith the stelar cylinder, forming a convex reticulum bridgingthe sides of the leaf gap. It is suggested that the characteristic stelar organizationof the Davalliaceae is derived by suppression of leaves froma radiallysymmetric dictyostele with spirally-arranged leafgaps as found in Nephrolepis and that Gymnogrammitis with itsreduced and suppressed leaves indicates the process of transition.The creeping solenostelic rhizome with two-ranked leaf arrangementcould be derived from an erectgrowing dictyostelic one by supppressionof leaves.     

Morphogenesis and its relation to architecture in the dimorphic clonal fern Lomagramma guianensis (Aublet) Ghing (Dryopteridaceae)

HEBANT-MAURI, R. & GAY, H., 1993. Morphogenesis and its relation to architecture in the dimorphic clonal fern Lomagramma guianensis (Aublet) Ching (Dryopteridaceae). The complex growth cycle of Lomagramma guianensis results from comparatively simple and uniform morphogenesis. The juvenile sporophyte is terrestrial, and assumes adult morphology upon becoming scandent. A single frondless runner is produced from the base of each monocarpic scandent rhizome base, and ramifies extensively on the forest floor. Moribund runners produce reiterative ramifications identical to the juvenile form, and these repeat the life cycle. All rhizomes share radial apical symmetry which becomes bilateral in differentiated tissues. Phyllotaxy is orthodistichous in sporelings and juveniles, and tristichous in adults. The vascular system of differentiated tissues is a variably stretched, perforated solenostele. The sporeling and inception of adult ramifications have solid protosteles, which become bilateral, vitalized and pierced by gaps resulting from departure of lateral meristem and frond traces. This transition from solid protostele to perforated solenostele facilitates reiteration and shows that a delay exists between formation of lateral meristems and their development. Cryptic extra-axillary meristems occur on adult rhizomes, which remain dormant on scandent rhizomes whilst the apex is alive, and subsequently develop fleetingly before axis death. They develop concomitantly with apex expansion in runners. A single type of lateral meristem produces the variety of adult and reiterated forms, regulated by its position on the axis, parent rhizome vigour and axis orientation.     

Ant colonization and coarse woody debris decomposition in temperate forests

Ants are ubiquitous, abundant and have widespread impacts on ecological communities and ecosystem processes. However, ant effects on coarse woody debris decomposition are unexplored. Several ant species colonize coarse woody debris for nesting, and this puts them in contact with fauna and microbes that utilize coarse woody debris as habitat and food, potentially influencing nutrient cycling and, ultimately, forest productivity. We report results from a field experiment employing 138 artificial ant nests (routed pine blocks) across five locations in southeastern US deciduous forests. We examine the correspondence between ant, termite and wood-eating fungi colonization and variation in coarse woody debris decomposition. After 1 year, nests colonized by ants had 5% more mass than those not colonized. Ant colonization corresponded with significantly less termite- and fungal-mediated decomposition of the nests. Without ants, termites removed 11.5% and fungi removed 4% more wood biomass. Ants, termites and wood-eating fungi all colonized pine nests where temperatures were highest, and ants also preferred higher soil moisture whereas termites and fungi responded negatively to high soil moisture when temperatures were higher. Ants reduce termite colonies through predation, and may inhibit fungi through the secretion of antimicrobial compounds. Our results indicate that interactions between forest understory ants, termites and fungi may influence the rate of coarse woody debris decomposition—biotic interactions that potentially influence forest structure and function.     

Poor Display Repertoire, Tolerance and Kleptobiosis: Results of Specialization in an Ant-Eating Spider (Araneae, Zodariidae)

The agonistic display repertoire of myrmecophagous Zodarion rubidum has five displays. This is fewer than in other spiders, which is a result of the short time spent in contests (4 s). Such a short duration seems to be an adaptation to living among foraging ants, which are dangerous to spiders. The interaction procedure was markedly affected by the presence of preyimmobilized ant. Contests between individuals without prey, or each holding prey, were usually resolved by leg waving. But contests between an individual without and an individual with prey escalated to more aggressive levels. Nevertheless, spiders were never observed to harm or cannibalize one another. Absence of cannibalism is explained as a result of diet specialization: only ants elicit a predatory behavior and provide Zodarion spiders with optimal nutrients. Some spiders used kleptobiosis to gain ants. They first tried to gain immobilized prey aggressively and if failed they adopted a stealthy tactic and shared the prey with the owner. Kleptobiosis is an alternative foraging strategy for Zodarion spiders as it reduces risks associated with hunting dangerous ants.     

CLONAL INTEGRATION: NUTRIENT SHARING BETWEEN SISTER RAMETS OF SOLIDAGO ALTISSIMA (COMPOSITAE)

To test whether sharing of resources occurs among connected ramets of the tall goldenrod, Solidago altissima, we examined the extent of clonal integration for nutrients. In a greenhouse experiment, two-ramet clones were grown in a triad of connected pots so that nutrients could be supplied to either sister ramet or to their old rhizome (mother rhizome). Mother rhizomes and their associated roots shared nutrients with daughter ramets; however, any nutrient sharing that occurred between sister ramets was too little to significantly affect their growth. In addition, sister ramets not only competed for nutrients through parental connections, but larger ramets inhibited the growth of smaller ramets. We suggest that, for tall goldenrod, a clonal growth strategy in which nutrients are not shared among sister ramets may increase genet fitness by reducing the rhizome production of ramets in poor-nutrient microsites. Consequently, the genet would produce relatively fewer ramets in unfertile areas and make better use of heterogeneous nutrient resources.     

Origin of Exogenous Adventitious Roots in Rhizomes of the Fern Microsorium scolopendria (Polypodiaceae)

Adventitious roots of rhizomes of the fern Microsorium scolopendriaarise exogenously from apical initials which have their originin the cell layer directly beneath the epidermis. Divisionsof the apical initial and its derivatives produce the adventitiousroot apical meristem. Cells between the apical cell and themeristele of the rhizome develop into the root trace. Anatomy, light microscopy, Microsorium scolopendria Burm.) Copel     

Dynamics of growth,carbon and nutrient translocation in Zizania latifolia

We studied the seasonal resource dynamics between organs of wild rice (Zizania latifolia (Griseb.) Turcz. ex Stapf.) to obtain a better understanding of its growth dynamics, carbon and nutrient translocation. The results of observation from January 2002 to February 2004 showed the shoot density markedly increased after emergence of shoots at the end of March until May (up to 800 ind/m²). However the shoot mortality due to self-thinning reduced the total new shoots by more than 70% by the end of July. Thereafter, the shoot density was nearly constant with the aboveground biomass peaking at the end of August. In the late winter, the rhizome biomass declined by respiration loss to about 25% of its peak value. Meanwhile the decline in rhizome reserves from January to the end of April was about 20%. This small reduction compared with other perennial emergent species implies that there is a lower contribution of rhizome reserves to support new shoot formation. The initial heterotrophic growth of new shoots based on the rhizome resources lasted for a short period, then switched to autotrophic growth at the end of April or the beginning of May. Thus, in most periods of foliage development, nutrients were obtained mostly from soil through uptake by roots, not through resource allocation of the rhizome. In autumn, the standing dead shoots retained most of the nutrients and carbohydrates without translocating downwards. This suggests that in practice, the plant can remove nutrients from sediment more efficiently than other emergent plants.     

Co-occurrence patterns of wood-decaying fungi and ants in dead pines of South Korea

Interaction between fungi and insects such as ants, beetles, wasps and termites inhabiting dead pine trees has significant ecological implication in the forest as they can decompose wood debris and add nutrients to the soil; however, only scarce information is available regarding the interaction between wood-decaying fungi and ants. We investigated wood-decaying fungi co-occurring with ants in dead pine trees of South Korea. A total of 57 pairs of wood-decaying fungi and ants were collected from 11 localities. 30 species of wood-decaying fungi and 14 species of ants were identified based on morphology and molecular analysis. Fungal species belonging to Trichaptum, Xylodon, Hyphodontia, and Ceriporia were dominant and co-occurred with common ant species of Lasius, Camponotus, Pristomyrmex, and Crematogaster across most of the sampling sites. This study provides a new baseline in unravelling the complex interaction between wood-decaying fungi and ants in forest ecosystems.