Dispersal potential of the invasive green alga Codium fragile ssp. fragile

Since its introduction in 1989, the invasive green alga Codium fragile ssp. fragile (formerly Codium fragile ssp. tomentosoides) has spread rapidly in Atlantic Canada. Although its spread has likely been facilitated by human transport, C. fragile possesses diverse modes of natural dispersal. In addition to parthenogenetically developing swarmer cells, it can propagate through the release of vegetative buds, thallus fragments, and entire, dislodged thalli. We examined the natural dispersal potential of these propagules using a combination of field and laboratory experiments. Vegetative buds were most abundant on thalli in late August, coinciding with increasing late summer wave activity. At two locations within two field sites, we examined the effects of tidal state, wave action and topography on the dispersal of fragments and intact thalli. Over a 4-hour period, retention rate was generally lower and dispersal distance of retained propagules higher: during flood than ebb tide; at the more wave-exposed locations; and for fragments than thalli. Dispersal direction corresponded with topography or flood tide currents at certain locations, but was often bi-directional or random, suggesting an added role of wave action. Over periods of weeks, the retention rate of marked detrital thalli was negatively related to the magnitude of wave activity. In the laboratory, settling rate was negatively related to propagule length, and large buds had higher critical shear erosional velocities than either small buds or fragments. Our results indicate that large propagules of C. fragile, such as intact adult thalli, have a generally low dispersal potential (meters), but may be transported longer distances (kilometers) during storms or when positively buoyant. Fragments and buds are regularly transported 10's of meters at a time at average flow velocities. However, they also become resuspended in average flows, and probably disperse longer distances over multiple resuspension events, or when positively buoyant. Once settled, the smallest propagules may be less easily resuspended or transported along the bottom as they become entrapped by small-scale topographic features or turf algae. The wide variety of propagules produced by C. fragile and the variable distances over which different propagule types may be transported give C. fragile the advantage of both short- and long-distance dispersal, and have likely played a role in the invasive success of this alga.     

DISPERSAL PATTERNS OF TERRICOLOUS LICHENS BY THALLUS FRAGMENTS

Dispersal patterns from seven terricolous lichen species, with a high capacity for asexual reproduction by fragmentation (Cetraria muricata, Cladonia species), were studied in differing vegetation types in north-eastern Germany. Marked lichen thalli were fragmented by trampling. After 15 days the spread of thallus fragments was monitored. Whereas most of the fragments that were dispersed by wind remained within a 20-cm radius from the source, the maximal dispersal distance was 57 cm in a dry sand grassland and 68 cm in an open pioneer pine forest. Dispersal was negligible in a closed old-growth pine forest. Several fragmented lichen cushions were disturbed and removed by animals, and led to a maximal dispersal distance of 9·70 m. These results suggest that: (a) thallus fragments provide good short-distance dispersal in open vegetation, but are inefficient for long-distance dispersal, and (b) wind and animals are important factors for the dispersal of thallus fragments. For restoration management of man-made substrata, artificial introduction of lichen thalli is proposed.     

Morphology influences water storage in hair lichens from boreal forest canopies

Hair lichens (Alectoria, Bryoria, Usnea) with high surface-area-to-mass ratios rapidly trap moisture. By photography and scanning we examined how internal water storage depended on morphological traits in five species. Specific thallus mass (STM, mg DM cm⁻²) and water holding capacity (WHC, mg H₂O cm⁻²) after shaking and blotting a fully hydrated thallus increased with thallus area. STM was ≈50% higher in Alectoria and Usnea thalli than in Bryoria. WHC was highest in Alectoria while percent water content of freshly blotted thalli was lowest in Usnea. Thallus area overlap ratio (TAO), assessing branch density of the thallus, was highest in the two thinnest Bryoria; lower in the thicker Usnea. Within species, hair lichens increased their water storage by increasing branch density rather than branch diameter. The taxonomically related genera Alectoria and Bryoria shared water storage characteristics, and differed from Usnea. Hair lichens in lower canopies have among the lowest water storage capacity reported in lichens.     

Post-fire recolonization of dominant epiphytic lichen species on Quercus hypoleucoides (Fagaceae)

Following a forest fire (27 500 ha) in 1994, post-fire recolonization of Quercus hypoeleucoides by epiphytic lichens was documented as changes in lichen cover, number of small thalli, specific factors that affected reestablishment of lichens, and modes of dispersal. Three sites in the Chiricahua Mountains (Arizona, USA) were chosen according to the severity of fire damage—unburned, moderately burned, and severely burned. From 1994 through 1997, the amount of dead lichen cover significantly increased at the moderately burned site. For the same time period, the amount of live lichen cover significantly increased at the severely burned site. Numbers of new thalli increased significantly at the severely burned site each year but only in the last year (1996–1997) for the moderately burned site. Bark texture and proximity to trees with lichens were among the most important physical factors for recolonization. The most important means of dispersal for Flavopunctelia praesignis was fragmentation. For Punctelia hypoleucites, the primary means of dispersal was spores. Increases in live lichen cover and numbers of new thalli occur faster in severely burned areas probably due to the loss of lichens on tree trunks, which provides space and a lack of competition.     

Further evidence that activation of net photosynthesis by dry cyanobacterial lichens requires liquid water

Abstract: In contrast to green algal lichens, cyanobacterial species of different families, growth forms and habitats proved to be unable to attain positive net CO₂ assimilation when the dry thalli were treated with air of high relative humidity; they needed liquid water for the reactivation of their photosynthetic apparatus. Identical behaviour is shown by all of the 47 lichen species with cyanobacterial photobionts, from six different genera, studied so far. This suggests a widely distributed, if not general, characteristic of cyanobacterial lichens. The difference in performance between both groups of photobionts was maintained when the lichen thallus was macerated. Furthermore, cultures of Chroococcidiopsis were unable to make use of water vapour hydration for positive net photosynthesis, and were similar in this respect to some free-living aerophilic cyanohacteria tested earlier. Possible physiological implications as well as ecological consequences for water-relation-dependent habitat selection of green-algal and cyanobacterial lichens are discussed.     

EFFECTS OF THALLUS DAMAGE ON INTERACTIONS OF LICHENS WITH NON-LICHENIZED FUNGI UNDER NATURAL AND LABORATORY CONDITIONS

The response of corticolous lichens to artificially induced chemical damage was compared to symptoms found on damaged lichens in the field. Experimental thalli were damaged and observed (1)in situin a relatively pristine area, and (2) in a growth chamber either hydrated continuously or periodically. Lichenicolous fungi encountered includedCornutispora lichenicola,Lichenoconium erodens,Phoma cytospora,Vouauxiomyces truncatus,Hobsonia christiansenii,Pronectria oligospora,Nectria rubefaciensand its anamorph,Acremonium rhabdosporum, and a variety of hyphomycetes. The results support the idea that both thallus necrosis and moist conditions are necessary to produce the full suite of symptoms observed on ailing lichens in the field.     

Seasonal acclimation in the epiphytic lichen Parmelia sulcata is influenced by change in photobiont population density

CO₂ gas exchange, radial growth, chlorophyll (Chl) content and photobiont density of an epiphytic population of Parmelia sulcata were monitored every 2 months during 1 year in a temperate deciduous forest of Central Italy, to verify possible seasonal variations. Light response curves of south-exposed thalli, built up in the laboratory at 6 and 27°C at optimal thallus hydration, showed that CO₂ gas exchange changed significantly during the year, with a maximum for gross photosynthesis in December at both temperatures. Photoinhibition phenomena occurred in early spring, immediately before tree leaves sprouted. The principal component analysis of CO₂ gas exchange parameters clearly separated the months with from the months without tree canopy cover. Radial growth, measured on marginal lobes of north- and south-exposed thalli, was the highest in December, and the lowest in April. Photobiont density, measured in lobes of south- and north-exposed thalli with a sedimentation chamber, also changed during the year: the number of photobionts was highest in June and December, and lowest in April, although no significant change in cell size and Chl content per cell was evident throughout the year. South-exposed thalli had slightly, but constantly higher photobiont density both on a weight and an area basis. The acclimation of lichen photosynthesis and Chl content to seasonal temperature and light changes should partially be re-visited on the basis of the significant variation in photobiont population density. This phenomenon still awaits, however, a satisfactory explanation, although it is probably related to the seasonal change in nutrient availability.     

Effects of enhanced UV-B radiation in the field on the concentration of phenolics and chlorophyll fluorescence in two boreal and arctic–alpine lichens

Lichens constitute a prominent part of the vegetation at high latitudes and altitudes, but the effects of UV-B radiation on these symbiotic organisms are not well known. In a northern boreal site (Abisko, northern Sweden), the usnic acid-producing lichens Flavocetraria nivalis and Nephroma arcticum were exposed to enhanced UV-B radiation, corresponding to 25% ozone depletion, for two and one growing seasons, respectively. They were compared with lichens grown under ambient UV-B and harvested fresh from the field. The treated thalli of F. nivalis had been transplanted from a site 24 km from the treatment site. From this source locality, untreated thalli were also harvested. Enhanced UV-B did not affect concentrations of usnic acid and the two depsides phenarctin and nephroarctin. A gradual decline of usnic acid, probably coupled to unusually long periods of dry, sunny weather, was observed both under enhanced and ambient UV-B and in untreated thalli. Photosystem II efficiency in both species was slightly reduced by enhanced UV-B. However, differences between seasons were larger than differences between treatments, which indicate that UV-B effects are minor in comparison to other climatic variables. Concentrations of UV-B-absorbing phenolics in lichens do not show a simple relationship to UV-B dose and therefore cannot be used as bioindicators of UV-B levels.     

Drag, drafting, and mechanical interactions in canopies of the red alga Chondrus crispus.

Dense algal canopies, which are common in the lower intertidal and shallow subtidal along rocky coastlines, can alter flow-induced forces in their vicinity. Alteration of flow-induced forces on algal thalli may ameliorate risk of dislodgement and will affect important physiological processes, such as rates of photosynthesis. This study found that the force experienced by a thallus of the red alga Chondrus crispus (Stackhouse) at a given flow speed within a flow tank depended upon (1) the density of the canopy surrounding the thallus, (2) the position of the thallus within the canopy, and (3) the length of the stipe of the thallus relative to the height of the canopy. At all flow speeds, a solitary thallus experienced higher forces than a thallus with neighbors. A greater than 65% reduction in force occurred when the thallus drafted in the region of slower velocities that occurs in the wake region of even a single upstream neighbor, similar to the way racing bicyclists draft one behind the other. Mechanical interactions between thalli were important to forces experienced within canopies. A thallus on the upstream edge of a canopy experienced 6% less force than it did when solitary, because the canopy physically supported it. A thallus in the middle of a canopy experienced up to 83% less force than a solitary thallus, and forces decreased with increasing canopy density. Thus, a bushy morphology that increases drag on a solitary thallus may function to decrease forces experienced by that thallus when it is surrounded by a canopy, because that morphology increases physical support provided by neighbors.     

Asymmetric Co-evolution in the Lichen Symbiosis Caused by a Limited Capacity for Adaptation in the Photobiont

It is proposed that lichen photobionts, compared to mycobionts, have very limited capacity to evolve adaptations to lichenization, so that the symbionts in lichens do not co-evolve. This is because lichens have (a) no sequential selection of photobiont cells from one lichen into another needed for Darwinian natural selection and (b) no photobiont sexual reproduction in the thallus. Molecular studies of lichen photobionts indicate no predictable patterns of photobiont lineages that occur in lichens so supporting this proposal. Any adaptation by photobionts accumulating beneficial mutations for lichenization is probably insignificant compared to the rate of mycobiont adaptation. This proposal poses questions for research relating the photobiont sexual cycle (genetic and cellular), the fate of photobiont lineages after lichenization, whether lineages of photobionts in thalli change with time, thallus formation by from spores as well as carbohydrate movement from photobionts to mycobionts and regulation of co-development of the symbionts in the thallus.     

Spatial variation in carbon isotope discrimination across the thalli of several lichen species

Variations in stable carbon isotope discrimination (δ) were investigated across the thalli of several lichen species possessing different photobiont associations. Lichens containing (i) green algae (phycobiont), (ii) green algae in association with cyanobacteria confined in cephalodia, or (iii) cyanobacteria (cyanobiont) as the photobiont partner were studied. Carbon isotope discrimination was analysed in different thallus sections, which varied in distance from the margin and in age. The marginal thallus region is considered to be youngest, while the central region is thought to be oldest. This analysis showed a clear variation in δ across the thallus related to distance from the growing margin. In most of the species examined, the highest δ values were found in marginal regions (younger), while the central and basal regions (older) showed significantly lower δ. To investigate the effects of the historical increase in atmospheric CO₂ concentration and the concurrent decrease in the ¹³C content of atmospheric CO₂ on the δ of lichens, experiments were carried out on herbarium samples of Lobaria pulmonaria collected from the mid 19th Century to 1953. The results obtained showed a pattern of variation of δ consistent with that of freshly collected samples; δ decreased substantially with increasing distance from the thallus margin, irrespective of the collection date. Moreover, no consistent variation of discrimination was found among different collection dates. These results demonstrate that the observed variation in δ is caused by age-related changes in the physiological behaviour of different thallus sections, and that the past 150 years of increasing CO₂ concentration have not had significant effects on A in L. pulmonaria. Photosynthesis measurements, chlorophyll analysis and observations using optical microscopy, performed on freshly collected lichens, showed significant changes in morphological and physiological characteristics across the thallus. Particularly, remarkable variations in thickness were found across the thallus. These anatomical changes may be responsible for the variation in δ, through variations in CO2 transfer resistance and, consequently, in CO₂ availability across the thallus. The lack of age-dependent variation in δ in cyanobiont lichens is possibly attributable to the operation of a CO₂-coneentrating mechanism and, therefore, to a more constant CO₂ environment across the thallus in this lichen group.     

Dew as a key factor for the distribution pattern of the lichen species Teloschistes lacunosus in the Tabernas Desert (Spain)

The role of different sources of water (rain, dew and water vapor) has been investigated under natural conditions in order to explain the activity and the distribution patterns of Teloschistes lacunosus (Rupr.) Sav. in the Tabernas Desert (Almeria, Spain). This field work was carried out at two neighboring sites: a pediment where T. lacunosus is well developed and an east-facing slope where only few small thalli are developed. Diurnal courses of photosynthetic activity were assessed by the use of chlorophyll a fluorescence measurements, at each site for a total of 12 days distributed among different seasons over the year. Microclimatic data (thallus temperature, relative humidity (RH) and light intensity) were recorded continuously for a period of 1 year including all the days on which fluorescence measurements were made. Dried T. lacunosus in its natural habitat only became photosynthetically active after re-hydration with liquid water (dew or rain). In contact with an atmosphere of high RH (higher than 90%) but without dew condensation, thalli were not able to obtain sufficient water to become physiologically active. The microclimatic study showed notably differences between the two studied expositions. After dawn, thalli from the east-facing slope were exposed to higher temperatures and light intensity (PPFD) levels than thalli from the pediment. This was reflected in the length of time that the air remained saturated and the lichen remained wet and active. The high incident PPFD and the resultant increased temperatures at the east-facing slope led to short dew duration and, therefore to shorter periods of morning photosynthetic activity than on the pediment as fluorescence measurements showed. Additionally, the microclimatic differences between the two sites indicated a high frequency of dew fall events on the thalli from the pediment. The time periods of thallus dew imbibition vary strongly with the exposure of the lichens.     

Fungal depsidones – an inducible or constitutive defence against herbivores in the lichen Lobaria pulmonaria?

Herbivore-deterrent depsidones in the epiphytic lichen Lobaria pulmonaria were quantified after a 104-day exposure to indigenous lichen-feeding mollusc communities in broadleaved deciduous forests in southeastern Norway. Controls and acetone-rinsed living thalli were transplanted under open and shaded tree canopies. Rinsed thalli had their depsidone concentration reduced to 36% of the pre-rinsing level, which is below the level needed to deter grazing molluscs. Grazing did not raise the concentration of depsidones beyond the level occurring in control to which molluscs had no access. Inducible responses were not detected in controls nor in acetone-rinsed thalli. Depsidone resynthesis was negligible in acetone-rinsed thalli regardless of grazing and/or light regimes. Our results suggest that C-based depsidones represent a constitutive type of herbivore defence in L. pulmonaria. A constitutive defence is probably an advantage for stress-tolerant slow-growing lichens inhabiting habitats with a constant presence of generalist invertebrate herbivores.     

Do secondary substances in the thallus of a lichen promote CO2 diffusion and prevent depression of net photosynthesis at high water content?

Many lichens show seriously depressed net photosynthesis (NP) at high thallus water contents due to increased carbon dioxide diffusion resistance through blockage of diffusion pathways by water. The soil lichen Diploschistes muscorum, however, shows no depression and NP is close to maximal even at the highest thallus water content. We investigated whether lichen substances (lecanoric and diploschistesic acids) in the cortex and medulla contributed to this ability to maintain high NP. Dry thalli were extracted with water-free acetone and, after this treatment, were found to be fully viable to the extent of continued growth after replanting in the field. No differences were found in the response of NP to thallus water content between the normal and extracted thalli, in fact the response curves were often nearly identical. Thus, in this species it seems that lichen substances did not maintain the water-free diffusion pathways and some other explanation, possibly structural, needs to be sought. Received: 5 April 1997 / Accepted: 26 April 1997     

The advantage of growing on moss: facilitative effects on photosynthetic performance and growth in the cyanobacterial lichen Peltigera rufescens

Facilitative effects and plant-plant interactions are well known for higher plants, but there is a lack of information about their relevance in cryptogams. Additional information about facilitative effects between bryophytes and lichens would be an important contribution to recent research on positive plant-plant interactions, as these can have striking influences not only on the organisation of early successional terrestrial communities but also on succession dynamics by kick-starting ecosystem development through the import of key nutrients. We investigated and quantified these mechanisms between Peltigera rufescens and its associated mosses. Moss-associated thalli had a different morphology that led to several benefits from the association. They had 66% higher net photosynthetic rate and, because the majority of the gas exchange of lichen thalli took place through the lower surface, there was a further increase as the CO(2) concentration was >25% higher beneath moss-associated thalli. Microclimatic measurements showed that mean light levels were substantially lower and temperature extremes slightly ameliorated for moss-associated thalli. As a consequence, desiccation was slower which is, together with an increase in thallus thickness and water storage, the reason for extended periods of optimal net photosynthesis for the moss-associated thalli. All these benefits combined to produce a growth rate of the moss-associated thalli which was significantly higher, twice that of non-associated thalli [0.75 ± 0.4 vs. 0.30 ± 0.1 mm/month (mean ± SD)]. This appears to be the first demonstration of a strong mechanistic basis for facilitative effects between lichens and bryophytes.     

Transplantation of lichen thalli: a case study on Cetraria islandica for conservation and pharmaceutical purposes

Changes in biomass growth and chemical composition of transplanted Cetraria islandica lichen thalli were investigated in a natural stand in the Bory Tucholskie region (northern Poland) over 3 yr. Transplants consisted of either 3.85 or 7.88 g fragments, 12.62 g clumps, or control plots where all vegetation and lichens were removed. The initial mass of C. islandica significantly influenced the percentage cover of investigated lichens at the study plots. At the last set of study measurements the highest cover, biomass accumulation (4×) and mean final mass (31.99 g m⁻²) of C. islandica were recorded at the study plots at which 7.77 g fragments were transplanted. Analysis showed that the content of the determined chemical compounds in each sample were similar. The potential influence of other species growing at the study area on the occurrence of C. islandica was also examined through monitoring species diversity in the cleared forest floor plots. Altogether 18 species of plants and lichens were recorded in study plots, and among most abundant species Dicranum polysetum and Pleurozium schreberi were observed. The mean percentage cover for C. islandica was 14.61 %.     

Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses

Dispersal of symbiotic partners by joint propagules is considered as an efficient strategy to maintain successful associations and to circumvent low symbiont availability. Joint dispersal is widespread in diverse symbioses and a particularly common reproductive mode in lichens. We were interested in the implications of joint symbiont dispersal on population genetic structure and investigated patterns of symbiont association in populations of two closely related lichen species in the genus Physconia, with similar range of compatible algal partners. One of the lichen species is characterized by joint dispersal of both symbionts, whereas the other species propagates by meiotic fungal spores alone. The latter species must re-establish the symbiotic stage with appropriate algae sampled from the environment. Both fungal species have specialized on photobionts representing a monophyletic lineage of the algal genus Trebouxia. The results indicate no correlated association of symbiont genotypes in the species with joint symbiont dispersal. We rather show that algal gene diversity in populations of lichenized fungi with different propagation strategies is not necessarily different. The association with algae that differ from the co-dispersed genotypes during the vegetative development of the thalli is the most likely explanation for the observed pattern. Maintenance of symbiotic associations is an option but not a strict consequence of joint symbiont dispersal in lichens.     

Phenology and thallus size in a non-native population of Gracilaria vermiculophylla

Phenology, or seasonal variation in life cycle events, is poorly described for many macroalgal species. We describe the phenology of a non-native population of Gracilaria vermiculophylla whose thalli are free-living or anchored by decorating polychaetes to tube caps. At a site in South Carolina, USA, we sampled 100 thalli approximately every month from January 2014 to January 2015. We assessed the reproductive state and measured thallus size based on wet weight, thallus length, and thallus surface area from herbarium mounts. Because life cycle stage cannot be assigned using morphology, we implemented a PCR assay to determine the life cycle stage—tetrasporophyte, female gametophyte, or male gametophyte—of each thallus. Tetrasporophytes dominated throughout the year, making up 81%–100% of thalli sampled per month. Reproductive tetrasporophytes varied between 0% and 65% of monthly samples and were most common in warm summer months (July through September) when thalli also tended to be larger. The vast majority of the reproductive thalli were worm-anchored and not fixed to hard substratum via a holdfast. Thus, free-living thalli can be reproductive and potentially seed new non-native populations. Given G. vermiculophylla reproduction seems tied closely to temperature, our work suggests phenology may change with climate-related changes in seawater temperatures. We also highlight the importance of understanding the natural history of macroalgae to better understand the consequence of range expansions on population dynamics.     

Lobe formation and division in the foliose lichen <Emphasis Type="Italic">xanthoparmelia conspersa</Emphasis>

New lobe development and lobe division was studied in the foliose lichen Xanthoparmelia conspersa (Ehrh. ex. Ach.) Hale. In thalli with either the centre or margin removed, the inside edge of the perimeter, the outer edge of the reproductive centre, and fragments derived from the thallus perimeter all regenerated growing points (‘lobe primordia’) within a year. Thalli possessing isidia had the greatest ability to regenerate growing points. In reproductive thalli, there was a positive correlation between the density of new growing points and thallus size. When fragments were cut from the perimeters of mature X. conspersa thalli and glued to pieces of slate, the ratio of growing points to mature lobes increased over 54 months. Lobes within a thallus exhibited different degrees of bifurcation. In some bifurcating lobes, the point of origin of the bifurcation advanced at the same rate as the lobe tips over 4 months but in most lobes, the bifurcation point either advanced less rapidly than the lobe tips or retreated from its original location. Removing adjacent lobes had no significant effect on the radial growth of a lobe over 4 months or on the location of the bifurcation point but it increased the number of growing points. These results suggest that for X. conspersa: 1) all portions of of thalli can regenerate growing points, 2) few growing points actually develop into mature lobes, 3) individual lobes within a thallus grow and divide differently, and 4) adjacent lobes inhibit the development of growing points on their neighbours.     

Competitive behaviour of umbilicate lichens – an experimental approach

The lichens Lasallia pustulata and Umbilicaria spodochroa grow in dense monospecific or mixed populations on the coastal cliffs of southern Scandinavia. Attached to the substrate by only a thin central holdfast, their shield-shaped thalli compete for light and space for growth by overlapping each other. Matched pair experiments in the laboratory and field observations of interacting pairs show that different behavioural responses to precipitation tend to result in the margins of U. spodochroa overlapping those of L. pustulata within a few minutes. The behaviour is apparently caused by different capacities for water absorption in the upper and lower cortices of the species. An initial period of repeated encounter caused by thallus expansion and contraction during precipitation will be followed by a period in which U. spodochroa grows to overlap L. pustulata more and more. When the overlapping lichens are wet, flexible and photosynthetically active, the thallus above rests directly on the upper surface of the one below. Very little light is transmitted through thalli of U. spodochroa, and the shaded parts of L. pustulata are retarded in their growth and die off. Received: 29 August 1996 / Accepted: 19 April 1997