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.     

EFFECTS OF NITROGEN AND PHOSPHORUS LEVELS,AND FROND-HARVESTING ON ABSORPTION,TRANSLOCATION AND ACCUMULATION OF ARSENIC BY CHINESE BRAKE FERN (PTERIS VITTATA L.)

This hydroponic experiment was conducted to determine the effects of nitrogen (N) and phosphorus (P) levels and frond-harvesting on the effectiveness of arsenic (As)-hyperaccumulator Chinese brake fern (Pteris vittata L.) to remove As from contaminated groundwater collected from south Florida. Three-month old ferns were grown in 38-L plastic tanks (two ferns per tank) containing 30-L of As-contaminated water (130 μg·L^?1 As), which was amended with modified 0.25 strength Hoagland's solution #2. Two N (26 or 52 mg·L^?1) and two P levels (1.2 and 2.4 mg·L^?1) were tested in one experiment, whereas the effect of frond-harvesting was tested in a separate experiment. Initially, N had little effect on plant As removal whereas low P treatment was more effective than high P and As was reduced to <5 μg·L^?1 in 28 d compared to 35 d. For well-established ferns, N and P levels had little effect. Reused fern, with or without harvesting the As-rich fronds, took up arsenic more rapidly so the As concentration in the groundwater declined faster (130 to ～10 μg·L^?1 in 8 h). Regardless of the treatments, most As (85–93%) was located in the aboveground tissue (rhizomes and fronds). Frond As concentrations were higher for non-harvested ferns than for ferns where fronds were partially harvested prior to treatment. Conversely, rhizomes accumulated more arsenic in ferns where fronds had been partially harvested. Low-P treatment coupled with reuse of more established ferns with or without harvesting fronds can be used to effectively remove arsenic from contaminated water using P. vittata     

The influence of extrafloral nectaries on parasitism of an insect herbivore

The extrafloral nectaries of many plants promote ant defense against insect herbivores. We examined the influence of extrafloral nectaries on the levels of parasitism of a generalist insect herbivore, the gypsy moth (Lymantria dispar L.). Larvae and pupae of the moth were collected from trees with and without extrafloral nectaries growing in the same forests in South Korea and reared to evaluate parasitism. More parasitism occurred on plants with extrafloral nectaries in seven of the nine season-long collections at the six sites and in four out of five collecting periods. Parasitism was higher on the four main genera of plants with extrafloral nectaries than on any of five main genera of plants without extrafloral nectaries. There was no difference in parasitoid richness; nine species occurred in each group, eight of which were the same. There was a positive and almost significant correlation between the abundance of plants with extrafloral nectaries and the parasitism of gypsy moth at the sites. Extrafloral nectaries may reduce herbivory by inducing more parasitism of the insect herbivores that attack plants bearing the glands.     

A Monographic Revision of the Fern Genus Neolepisorus Ching

The genus Neolepisorus Ching was proposed in 1940 and then consisted of five species including the type, Polypodium ovatum Wall. ex Hook. et Grev. The generic sense of Neolepisorus is now more homogenour than originally constructed. Strictly speaking, the genus then had only three species: Polypodium ovatum Wall. ex Hook. et Grev. of the Himalayas and China, P. ensatum Thunb. of Japan, and China, and P. lastii Baker of Africa (Madagascar). Since then our knowledge of the genus has substantially been enriched, as there are now 10 species known from China as described in the present paper. Phylogenetically, the genus Neolepisorus is a natural one in the family Polypodiaceae, beiny closely related to Nicrosorium Link, Calysis Presl and Tricholepidium Ching in general habit, scale structure, spores and chromosome numbers (x = 36), while its affinity with the genus Lepisorus (J. Sm.) Ching is much less close in these respects. From its related genera Neolepisorus differs in terestrial habit,typically long-stipitate simple fronds, distinct lateral main veins with 1--3(4) striate and irregularly dispersed sori covered when young with angular, clathrate and long-stalked paraphyses. One marked morphological peculiarity of the genus Neolepisorus is, however, that the fronds in many species from Guizhou and Sichuan are so divided into more or less similarly pinnatifid or lobed monstrous shapes that their proper identity is frequently indiscernible--a character not yet seen in ferns of other genera in China at least. It offers an interesting research subject for the morphologists. Geographically, the genus Neolepisorus is mainly Chinese. Except one species endemic to Afrira (Madagascar), one in Indo Himalayas, upper Burma, nothern Thailand, Indo-China and China and the third species in Japan and China, all are found endemic to China,northwards to the southern part of Shaanxi (Shensi) Province, south of the Tsing-ling Range. Ecologically, they all prefer half-sunny floor under secondary forests or among shrubberies.     

Seasonal and interspecific variation in the biochemical composition of some British fern species and their effects on Spodoptera littoralis larvae

Fern-feeding insects in Britain are mainly found on mature fronds in late summer. Six fern species (Dtyopteris filix-mas, D. dilatata, D. borreri, Phyllitis scolopendrium, Polyslkhum setiferum and Polypodium vulgare) were analysed for fibre, lignin, cellulose, tannins, cyanogenesis and thiaminase activity in an attempt to determine the biochemical basis for this seasonal pattern of attack. A bioassay was also carried out, using frond material incorporated in the diet of Spodoptera littoralis, to determine the effects of seasonal changes in fern toxins on a non-adapted, insect herbivore. The young fronds of all six species had a high protein content and low fibre-lignocellulose; protein levels decreased and cell wall materials increased as the fronds matured. Tannin concentrations and thiaminase activity showed a less consistent seasonal pattern. Tannins were present in the highest concentration in the young fronds of D. borreri, Polystichum and Polypodium and decreased with season; D. dilatata, Polystichum and Polypodium showed a similar pattern of thiaminase activity. The other species showed no strong seasonality in the levels of either tannins or thiaminase. No cyanogenic activity was detected in any of the fern species. Frond material from all six species decreased survivorship and growth rates of Spodoptera larvae. Larval performance and growth on diets containing fern material from young immature fronds was generally poorer than on diets containing material from mature fronds, collected later in the season. Neither tannin concentrations nor thiaminase activity levels closely corresponded to the observed interspecific and seasonal patterns of larval development and mortality, and other toxins must be involved. It is concluded that ferns are highly toxic to non-adapted herbivorous insects but the effects on adapted species are unknown. The restricted seasonal occurrence of a small number of insect species exhibiting specialized feeding habits suggests, however, that biochemical properties of the ferns determine this pattern of attack and limit the number of species which are able to exploit ferns as food resources.     

Characteristics of Arsenic Accumulation by Pteris and non-Pteris Ferns

This research was conducted to understand the mechanisms of arsenic hyperaccumulation in Pteris vittata by comparing the characteristics of arsenic accumulation in Pteris and non-Pteris ferns. Seven Pteris (P.vittata, P. Cretica Rowerii, P. Cretica Parkerii, P. Cretica Albo-lineata, P. Quadriavrita, P. Ensiformis and P. Dentata) and six non-Pteris (Arachnoides simplicor, Didymochlaena truncatula, Dryopteris atrata, Dryopteris erythrosora, Cyrtomium falcatum, and Adiantum hispidulum) ferns were exposed to 0, 1 and 10 mgL⁻¹ arsenic as sodium arsenate for 14-d in hydroponic systems. As a group, the Pteris ferns were more efficient in arsenic accumulation than the non-Pteris ferns, with P. vittata being the most efficient followed by P. cretica. When exposed to 10 mg L⁻¹ As, arsenic concentrations in the fronds and roots of P. vittata were 1748 and 503 mg kg⁻¹. Though not all Pteris ferns were efficient in accumulating arsenic, none of the non-Pteris ferns was an efficient As accumulator (the highest concentration being 452 mg kg⁻¹). The fact that frond arsenic concentrations in the control were highly correlated with those exposed to As (r ² = 0.76–0.87) may suggest that they may be used as a preliminary tool to screen potential arsenic hyperaccumulators. Our research confirms that the ability of P. vittata to translocate arsenic from the roots to the fronds (73–77% As in the fronds), reduce arsenate to arsenite in the fronds (>50% AsIII in the fronds), and maintain high concentrations of phosphate in the roots (48–53% in the roots) all contributed to its arsenic tolerance and hyperaccumulation.     

No Defensive Role of Ants throughout a Broad Latitudinal and Elevational Range of a Cactus

Defensive mutualisms mediated by extrafloral nectaries are particularly variable; their net results may change with seasons, communities and environmental contexts. Particularly, an environmental factor that can promote changes in outcomes of ant‐plant interactions is elevation in mountainous regions. We tested whether (1) the interaction between the cactus Opuntia sulphurea and ant visitors of extrafloral nectaries is a defensive mutualism; and (2) ant‐plant interaction outcomes vary with elevation as a result of changes in herbivory rate and ant activity. To evaluate if the outcome of interactions was consistent at two extremes of the range distribution of O. sulphurea, we performed an ant‐exclusion experiment with plants at two growth conditions (natural or potted) in two sites with contrasting elevation (1235–1787 m asl) in a temperate region (Villavicencio Nature Reserve, Mendoza, Argentina), and in a tropical region (Huajchilla, La Paz, Bolivia). Although herbivory rate and ant visitation frequency increased with elevation, herbivore damage, plant reproductive success, and cladode growth rate were similar between plants excluded and non‐excluded from ants among sites, geographic regions and growth conditions. These results do not support the hypotheses that the interaction between O. sulphurea and ants is a defensive mutualism, and that elevation affects the net outcome of this ant‐plant interaction.     

Early-spring gas exchange and uptake of deuterium-labelled water in the poikilohydric fernPolypodium virginianum

This study was carried out to determine if the desiccation-tolerant fernPolypodium virgimanum L. ecologically resembles lower plants by absorbing atmospheric water through its fronds and actively growing in early spring when the soil along cliff edges is still frozen. Three times between February and April, 1991,P. virginianum clonal mats were treated with deuterium-labelled water. Following each application, fronds were collected over several days and analyzed for the presence of deuterium. Two treatment groups plus a control were used: fronds were sprayed directly while covering the soil, or the roots were watered while protecting the fronds. The control mats were left untreated. Soil, air, and frond temperatures, plus photosynthesis and frond conductance were monitored throughout the study period. At subfreezing temperatures in February, no labelled water was taken up from the soil and no photosynthesis took place. Small amounts of label were absorbed from the soil in March during freeze-thaw cycles when rates of photosynthesis and stomatal conductance were both low. Large amounts of label were taken up from the soil in April when the soil was fully thawed and gas exchange was at normal seasonal levels. Label was not absorbed directly through the fronds when the plants were actively growing. Despite the desiccation tolerance ofP. virginianum, the timing and patterns of its water uptake and gas exchange in early spring resemble those found in higher vascular plants, not poikilohydric lower plants.     

Ant Defense Versus Induced Defense in Lafoensia pacari (Lythraceae), a Myrmecophilous Tree of the Brazilian Cerrado1

We compared the effects of ant presence at extrafloral nectaries of Lafoensia pacari St. Hil. on herbivore damage and silicon accumulation. Plants that were accessible to ants experienced lower herbivory levels over the first 3 mo of the experiment. After 3 mo, most leaves were fully expanded with inactive extrafloral nectaries; by 6 mo there was no effect of ant access on herbivore damage. Along with experiencing higher herbivory, plants in the ant‐exclusion treatment had significantly higher silicon levels in their leaves, suggesting that silicon serves as an induced defense in this ant–plant–herbivore interaction.     

The role of extrafloral nectaries in the herbivore defence of Cassia fasiculata

Abstract. 1. An experiment is presented that tests the hypothesis that the extrafloral nectaries of Chssia fasiculata reduce herbivory by attracting pugnacious ants that deter herbivores, and tests the equivalence of two methods of ant exclusion: treatment with Tanglefoot, and nectary excision.
2. The protectionist hypothesis is not supported; treatment plants produced as many pods as did control plants.
3. Treatment with Tanglefoot is equivalent to nectary excision in terms of pod production
4. A graphical model is presented that relates the efficacy of ant protection to plant density and ant activity.     

Ultrastructural changes in rhizome parenchyma of <Emphasis Type="Italic">Polypodium vulgare</Emphasis> during dehydration with or without abscisic acid pretreatment

Common polypody (Polypodium vulgare L.) belongs to desiccation-tolerant ferns. The structure of storage parenchyma of their rhizome was examined by transmission electron microscopy after dehydration and subsequent rewetting. Analysis revealed that treatment with supplemental abscisic acid resulted in protection of cells against ultrastructural damage compared to untreated ones. Dehydration rate appears to modify the ability of rhizome parenchyma to stand water stress.     

Invasive feral pigs impact native tree ferns and woody seedlings in Hawaiian forest

Invasive mammals can fundamentally alter native plant communities, especially on isolated islands where plants evolved without them. The globally invasive feral pig (Sus scrofa) can be particularly destructive to native plant communities. Tree ferns are an important understory component in many forests facilitating the establishment of a variety of species. However, the extent and effects of feral pig damage to tree ferns, and associated impacts on plant community regeneration, are largely unknown. We quantified the effect that feral pig damage has on tree fern growth, survival, and epiphytic woody seedling abundance over 1 year on 438 randomly selected tree ferns of three endemic species (Cibotium chamissoi, Cibotium glaucum, and Cibotium menziesii) in a Hawaiian montane wet forest with high tree fern and feral pig densities. Across all tree fern species, feral pigs damaged 13 % of individuals over 1 year. Compared with undamaged tree ferns, moderately- to heavily-damaged individuals had decreases of 4 to 27 % in trunk length increment and lost tenfold more fronds. Tree fern angle (standing, leaning, prone, or semi-prone) and woody seedling abundance co-varied with feral pig damage. Specifically, damaged tree ferns were more often prone or semi-prone and supported more seedlings, but also had annual mortality up to 34 % higher than undamaged tree ferns. Overall, feral pig damage had substantial negative effects on tree ferns by reducing growth and survival. Given the importance of tree ferns as regeneration sites for a variety of native plants, feral pig damage to tree ferns will likely alter future forest composition and structure. Specifically, feral pig damage to tree ferns reduces potential establishment sites for species that either regenerate preferentially as epiphytes or are currently restricted to epiphytic establishment due to ground rooting by feral pigs.     

Plant-attracted ants affect arthropod community structure but not necessarily herbivory

Abstract.  1. The effectiveness of ants as plant defenders is equivocal for plants that attract ants via extrafloral nectaries (EFNs).
2. This study focused on the myrmecophilic savannah tree Pseudocedrela kotschyi that attracts ants to EFNs and on the arthropod fauna associated with P. kotschyi . Herbivory and arthropod community composition were compared between trees that were dominated by one of three congeneric ant species, Camponotus acvapimensis , C. rufoglaucus , and C. sericeus , and between trees where ants were experimentally excluded and untreated control trees.
3. Short-term ant-exclusion experiments failed to demonstrate a consistent effect of ants on herbivory.
4. Plants dominated by different ant species differed significantly in leaf damage caused by herbivorous insects. The relative ranking of herbivory levels of the trees dominated by different ant species was persistent in three consecutive years.
5. Ants significantly reduced the abundance of different arthropod groups (Araneae, Blattodea, Coleoptera, Homoptera, non-ant Hymenoptera). Other groups, including important herbivores, seemed not to be affected (Lepidoptera, Orthoptera, Thysanoptera, Heteroptera).
6. The study suggests that the presence of ants only benefits plants when specific ant species are attracted, and protection by these ants is not counterbalanced by their negative effect on other beneficial arthropods.     

Public goods,public services and by‐product mutualism in an ant–fern symbiosis

Mutualism can evolve when organisms make novel connections that happen to benefit all parties. When such connections involve a host that provides a public good for multiple visitor species, selection for reciprocal cooperation is only likely if the host has the power to preferentially increase the fitness of those visitors that provide a better quality service. In contrast, when interactions form between multiple visitors and a host that lacks the power to partition the public good, we predict that interactions are likely to persist only as by‐product mutualisms, in which symbiosis benefits both host and visitor, but in which neither partner makes costly investments. Focusing on the symbiosis between ants and litter trapping epiphytes in the canopy of lowland dipterocarp rain forest in Borneo, we show that at least 71 ant species share the public good of housing within the root‐mass of epiphytic bird's nest ferns (Asplenium spp.). Ferns supporting a higher biomass of ants experienced less herbivory, and experimental exclusions of ants from fronds confirmed that this is caused by the ants protecting the ferns from herbivores. These results establish that there are clear by‐product benefits for both parties of housing for ants and protection for ferns. If these benefits were to drive selection for reciprocal cooperation, we would expect larger ferns to support ant colonies that were larger or colonies that produce more reproductive individuals. This was not the case. Larger ferns instead supported more ant colonies, indicating that the housing provided by the fern is a public good that is not restricted to better cooperating ant species. Mutualism via novel connections is thus unlikely to evolve between a host and multiple partners, even if there are clear by‐product benefits to all parties, unless the host can direct benefits to cooperators.     

FOSSIL EXTRAFLORAL NECTARIES,EVIDENCE FOR THE ANT-GUARD ANTIHERBIVORE DEFENSE IN AN OLIGOCENE POPULUS

Extrafloral nectaries are secretory glands, usually found on leaves, that have been shown to promote ant defense against the insect herbivores of many modem day plants. Extrafloral nectaries were found on the 35-million-year-old fossil leaves of the extinct Populus crassa from Florissant, Colorado. Extinct ant species (belonging to five still extant genera that have modem ant-guard species), and other predators and parasitoids (whose modem relatives frequent extrafloral nectaries) also lived at Florissant. The extrafloral nectaries of P. crassa (and perhaps other plants) probably operated to attract ants and/or other arthropod defenders as early as the Oligocene.     

Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation

Abstract. 1. Ants (Myrmica spp. and Formica lemani) visiting the extrafloral nectaries of bracken, Pteridium aquilinum, imposed heavy mortality on caterpillars of a novel moth species experimentally introduced onto bracken fronds. However, the exclusion of ants from bracken fronds had no significant effect on adapted bracken-feeding herbivores in Britain.
2. The feeding stages of British bracken-feeding insects are immune to, or can largely avoid, predation by ants in a variety of ways. Gall formers and miners cannot be attacked by these ants. Two other species hide, one inside tied leaves, the other in a mass of 'spittle'. Another group of species jumps away from, or falls off the plant when touched by ants. Sawfly caterpillars in the genera Strongylogaster, Aneugmenus and Tenthredo have viscous, distasteful haemolymph that repels ants.
3. No species of bracken herbivore has an absolute temporal refuge from ants; during their development they all overlap with ants to some degree.
4. Ant predation appears to have played a significant role in determining the contemporary structure of British bracken-feeding insect communities. Distasteful haemolymph in sawfly caterpillars may have evolved in response to selection from ant predation. Other species may fortuitously possess characteristics, evolved in response to a variety of selective forces, that also reduce the impact of ants; without such characteristics, however, we postulate that they would be unable to live on this plant. An absence of external, foliage feeding Lepidoptera early in the spring, a high proportion of sawfly species, and a high proportion of gall-formers and miners may all be characteristics of the bracken herbivore community which have been influenced by ant predation.     

Reiterative growth in the complex adaptive architecture of the Paleozoic (Pennsylvanian) filicalean fern Kaplanopteris clavata

Reiteration is a widespread component of plant growth whose evolutionary importance in ferns is not recognized widely. We introduce and discuss the growth architecture of Kaplanopteris clavata, a fossil filicalean fern from the Pennsylvanian (ca. 305 million yeas old), focusing on types of reiteration exhibited by this species and on the adaptive and phylogenetic significance of reiteration for ferns in general. Kaplanopteris clavata combines two types of reiterative growth where growth modules are borne on fronds: (1) entire fronds derived from primary pinnae, and (2) epiphyllous plantlets. This combination of reiterative pathways, unique among fossil and living ferns, allowed K. clavata to explore ecospace through an opportunistic combination of scrambling, climbing and epiphytic growth. Kaplanopteris clavata underscores the organographic importance of fronds (as opposed to stems) in the adaptive architecture of ferns, emphasizing functional convergences between the different Baupla̋ne of ferns and angiosperms. This unique combination of reiterative pathways is interpreted as a derived condition illustrating the structural and developmental complexity achieved by some filicaleans during the first major evolutionary radiation of leptosporangiate ferns.     

Testing for mycorrhizal fungi-plant-ant indirect effects

Abstract

Recent work has demonstrated indirect effects between mycorrhizal fungi and insect herbivores and pollinators. The existence of indirect effects between mycorrhizal fungi and protection-for-food mutualists, such as extrafloral nectar-foraging ‘bodyguard ants’, is unknown. In this study, we examined the potential for indirect effects of arbuscular mycorrhizal fungi on aggressive ant bodyguards, mediated by changes in the expression of extrafloral nectaries of a shared host plant. We found that mycorrhizal plants grew larger and produced more extrafloral nectaries compared to their non-mycorrhizal counterparts. The difference in the number of nectaries between mycorrhizal and non-mycorrhizal plants, however, was too small to elicit differences in ant attendance. In spite of the lack of a significant indirect effect of mycorrhizal fungi on ant attendance, mycorrhizal plants suffered damage to a significantly greater proportion of their leaves compared to non-mycorrhizal plants. This result likely stems from other (non-ant-mediated) indirect effects of mycorrhizal fungi on herbivores.     

Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae)

1. This study examines the anti-herbivore effect of ants visiting the extrafloral nectaries (EFNs) of Opuntia stricta (Cactaceae) and its possible influence on the plant's reproductive output in Mexican coastal sand dunes. Opuntia 's EFNs are located in the areoles of the developing tissue of emerging cladodes and flower buds.
2. Ants visited the EFNs of O . stricta on a round-the-clock basis. The associated ant assemblage was formed by nine species distributed in four subfamilies, and the species composition of the principal ant visitors changed markedly from day to night period.
3. Cladodes of control (ants present) and treatment (ants excluded) plants of Opuntia were equally infested by sucking bugs and mining dipterans. Damage to buds by a pyralid moth, however, was significantly higher on treatment than on control plants. Ant visitation to Opuntia 's EFNs translated into a 50% increase in the plant's reproductive output, as expressed by the number of fruits produced by experimental control and treatment branches. Moreover, fruit production by ant-visited branches was positively and significantly associated with the mean monthly rate of ant visitation to EFNs.
4. This is the first demonstration of ant protection leading to increased fruit set in the Cactaceae under natural conditions. Although the consequences of damage by sucking and mining insects remain unclear for Opuntia , the results show how the association of EFNs with vulnerable reproductive plant organs can result in a direct ant-derived benefit to plant fitness.     

FACULTATIVE MUTUALISM BETWEEN WEEDY VETCHES BEARING EXTRAFLORAL NECTARIES AND WEEDY ANTS IN CALIFORNIA

Vetches (Vicia spp.) were studied in the San Francisco Bay Area of California in the spring of 1978. The stipular nectaries of the vetches are visited by the Argentine ant, Iridomyrmex humilis Mayr. The nectaries were removed to exclude ants in controlled experiments to determine if these ants protect the vetches from herbivores or seed predators. Plants with excised nectaries suffered substantially greater damage to their foliage than control plants, indicating that ants protect the foliage. There was no indication that ants protect the vetches from seed predators, but fruit set was substantially lower in plants with excised nectaries. Analysis of sugar and amino acid composition of extrafloral nectar served as a basis for feeding tests with Argentine ants by using artificial nectar solutions. Ants preferred sucrose and glucose solutions over fructose. They showed no preference for any one sugar mixture over another, nor did they exhibit differential recruitment to artificial nectar solutions containing only sugars or sugars and amino acids.