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Keywords:

  • Antarctic flora;
  • Antarctica;
  • Colobanthus quitensis;
  • Cushion plants;
  • Deschampsia antarctica;
  • mosses;
  • Nurse plants;
  • Positive interaction;
  • Sanionia;
  • Usnea antarctica;
  • Usnea aurantiacoatra

Abstract

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

A recent article published by Molina-Montenegro et al. (Journal of Vegetation Science24: 463) examines the association of Antarctic native plant and lichen species to the lichen Usnea antarctica on Fildes Peninsula, King George Island, maritime Antarctica. The authors report that on two sites, five out of 13 and four out of 11 species of lichens and mosses were spatially associated with U. antarctica, suggesting positive interactions between them. Although Deschampsia antarctica does not grow naturally associated with U. antarctica, Molina-Montenegro et al. carried out a transplantation experiment to demonstrate that the macrolichen acts as a nurse plant, improving the survival of the grass. Serious conceptual and methodological discrepancies emerge from a critical evaluation of this study, challenging their conclusions. First, we suspect that the author confused some lichen taxa, and we also disagree with macrolichens being treated as cushion plants, because rootless, poikilohydric and poikilothermic thallophytes such as lichens are unable to create a stable, enclave-like microhabitat as vascular cushion plants do. Indeed, a critical evaluation of some of the micro-environmental parameters measured indicates that there are no biologically meaningful differences between the U. antarctica thalli and surrounding open areas. Second, the lack of consideration of the life history of the species under study leads to confusion when (a) referring to the succession sequence of species that colonize the studied area and (b) interpreting the putative distribution patterns promoted by Usnea versus the substrate preferences of associated species. Third, the authors intend to demonstrate experimentally that Usnea can facilitate the survival of D. antarctica plants, transplanting adult plants and not seedlings between the lichen thalli, and it is not clear how the grass was planted – between or within the lichens – as at both experimental sites the lichens grow on stones or rocks. Facilitative interactions are present in the Antarctic and may play a pivotal role in the structure and functioning of the fragile Antarctic ecosystems. However, more rigorous and well-planned research is needed to assess its presence, importance and involved mechanisms.

Molina-Montenegro et al. (2013), hereafter M-M et al. (2013), attempted to show that in the Antarctic, one of the most extreme environments for life, the macrolichen Usnea antarctica Du Rietz acts as a nurse plant, facilitating other native species including mosses, lichens and vascular plants (see also Callaway 2013). To make their case, the authors evaluated: (1) the frequency of other lichen and moss species growing associated with the lichen U. antarctica compared to adjacent lichen-free areas; (2) whether survival of seedlings of Deschampsia antarctica Desv. (Poaceae) is increased when planted within ‘cushions’ of U. antarctica compared to bare soil; and (3) how the presence of U. antarctica affects soil properties (temperature, nutrient availability and soil moisture). In our opinion, however, both the data set and the interpretation of the results presented by M-M et al. (2013) contain several important flaws that undermine their conclusions.

Studied species

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

Although M-M et al. (2013) refer to U. antarctica as a ‘nurse plant’ or ‘cushion plant’ and use the concept of ‘plant–plant interaction’ when postulating facilitation between U. antarctica and the associated species, lichens are predominantly fungal organisms and not plants. Their gross functional morphology is strongly dominated by the lichenized fungus (Øvstedal & Smith 2001). In contrast to the information provided by M-M et al. (2013), U. aurantiacoatra (Jacq.) Bory (syn. U. fasciata) is the most abundant species of Usnea along the maritime Antarctic (Lindsay 1971; Redón 1985; Andreyev 1989; Øvstedal & Smith 2001; Olech 2004) and particularly on Fildes Peninsula, whereas U. antarctica is the most widely distributed through the entire Antarctic, including the continental area. We suspect that the authors confused the two species, because in fig. 1 of M-M et al. (2013) it can be seen that the largest thalli correspond to U. aurantiacoatra, showing the typical large apothecia (10–20 mm diam.), whereas U. antarctica rarely produces apothecia in the Antarctic, those being also smaller (up to 10 mm diam.) and subterminally formed (Redón 1985; Øvstedal & Smith 2001; Seymour et al. 2007). Unfortunately, it is not mentioned in the paper on which base of expertise or references the species were identified, nor where voucher specimens were deposited, which would allow verification of the assigned names by a specialist. This is not trivial in an ecological context, because the two Usnea spp. are difficult to distinguish and there has even been some controversy whether U. aurantiacoatra and U. antarctica are separate species or just represent fertile and sterile conspecific morphs (Seymour et al. 2007); so a precisely defined taxonomical concept has to be used when competition between the two taxa is suggested, as in the article of M-M et al. (2013). That up-to-date lichen taxonomy has not been adequately applied by these authors also becomes evident in misplacement of U. aurantiacoatra in the family Usneaceae instead of Parmeliaceae (table 1 of the cited article).

According to M-M et al. (2013), macrolichens such as U. antarctica and U. aurantiacoatra form ‘cushions’ and the authors refer to lichens as cushion plants throughout the article. However, there are sharp differences between fruticose lichens such as Usnea spp., which are thallophytes, and typical vascular cushion plants –cormophytes – highly abundant in alpine and sub-polar tundra (Körner 2003). In contrast with lichens, plants are able to actively modify the temperature regime through regulation of evapotranspiration (Larcher 1995), and cushion plants are able to buffer temperature extremes, enhancing the formation and accumulation of organic matter and retention of moisture (Körner 2003; Cavieres et al. 2010; le Roux & McGeoch 2010) as a consequence of their compact form. Thus, the concept of facilitation by cushion plants has been developed based on the particular growth of vascular plants which separate a sheltered ‘interior’, enclave-like environment from the ‘exterior’ environment.

This concept is clearly not applicable in the case of the Usnea thalli addressed in the study of M-M et al. (2013): neither do these lichens form a closed canopy (as clearly visible on the site photograph in the article), nor do they include a root–soil compartment in the protected space. Lichens, by their very nature, are less differentiated, rootless, poikilohydric and poikilothermic organisms that are not capable of actively forming a discrete microhabitat with constant ‘inside’ conditions that are different from the ‘outside’ conditions, but are simply passively reacting to the microclimatic conditions of their growing site, which is clearly expressed in their periodic de- and rehydration (Pannewitz et al. 2003).

Association patterns

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

Scrutinizing the first objective of M-M et al. (2013), the sampling procedure contains some errors and omissions. The authors measured the frequency of association between the species growing on two different substrates, but did not indicate the abundance of these substrates in the study sites. Data analyses are based on the assumption that both substrates are equally abundant or available for colonization, which is unlikely. Further, neither frequency nor distribution of the different thallus size classes of U. antarctica and U. aurantiacoatra are indicated. Without such information, it could be assumed that the authors considered several Usnea thalli as one cushion, which could explain the large size of the so-called ‘lichen cushions’.

But a more important aspect is related to the substrata. M-M et al. (2013) differentiated between lichen thalli (‘cushions’) and bare ground as contrasting substrates. However, lichens grow preferentially on rocks, stones and mosses in this area (pers. obs.). Thus in this context, it is not possible to compare lichen species richness growing on stones with that of lichens growing on bare ground covered by pebbles, gravel or mosses, because these are different substrata per se, and not modified by the presence of a nurse species, as is implied by the authors' approach. For example, U. aurantiacoatra and U. antarctica are saxicolous species, as well as the crustose lichens Caloplaca sublobulata (Nyl.) Zahlbr., Rhizoplaca melanophthalma (DC.) Leuckert & Poelt, Placopsis contortuplicata I.M. Lamb, Rhizocarpon geographicum (L.) DC. and the foliose lichen Umbilicaria antarctica Frey & I.M. Lamb. In contrast, Cladonia metacorallifera Asahina, Stereocaulon alpinum Laurer, Psoroma hypnorum (Vahl) Gray grow on moribund mosses and cannot be found on stones or gravel. Polytrichum sp. is not a lichen, as incorrectly shown in table 1 of M-M et al. (2013), but a moss and prefers soil as substrate. Andreaea spp. can be either found on rocks and stones or on soil. The moss Brachythecium sp. grows only on soil, and not on gravel or rocks, as well as Sanionia sp., which grows on wet to flooded soil instead of stones, and probably between stones or in rock crevices. Thus, the positive spatial associations shown in M-M et al. (2013) correspond to substrate preference and not to facilitative interactions, as concluded by the authors. During 6 yrs of field research in the Antarctic, we have observed that Sanionia spp. form large carpets (>1000 m2) on wet soils of several sites along the Antarctic Peninsula, which explains the low number of individuals of these species found by the authors between the fruticose and crustose lichen communities (table 1 of M-M et al. 2013).

Substrate structure, and probably soil nutrient chemistry, is considered most relevant for lichen distribution and community structure (Hovenden & Seppelt 1995; Crittenden 1998; Kappen 2000). According to the colonized substrates, lichens can be classified as ornithocoprophilous (which are usually found on rocks or stones in the vicinity of nesting birds) and ornithocoprophobous (species that are found principally on rocks with little bird activity; Lindsay 1971; Øvstedal & Smith 2001; Olech 2004). Contrary to the report of M-M et al. (2013), of the 14 species listed in table 1, only five are associated with U. antarctica; three of them are ornithocoprophilous species (C. sublobulata, R. melanophthalma and Um. antarctica), which occur frequently with U. antarctica (Lindsay 1971), but P. contortuplicata and R. geographicum, as ornithocoprophobous species, do not co-occur with U. antarctica or U. aurantiacoatra. That is, the described association pattern should be explained principally by substrate requirements and not by the effect of microclimatic improvement suggested by the authors. The case of Cladonia metacorallifera is not really clear, because this species has not been described for the Fildes Peninsula area (Øvstedal & Smith 2001; Olech 2004). Øvstedal & Smith (2001) suggest that the taxon could be C. lepidophora (Flörke ex Sommerf.) Spreng., which is uncommon in the area, or C. borealis S. Stenroos, which is widespread and frequent on mosses, such as Andreaea spp. The other muscicolous species Stereocaulon alpinum and Psoroma hypnorum do not co-occur with U. antarctica due to the substrate requirements explained above, neither do the mosses Brachytecium sp., Polytrichum sp. and Sanionia sp. Finally, the positive association of Andreaea spp. is not backed up by the report of Øvstedal & Smith (2001), who indicate that U. antarctica occurs infrequently with this moss species, whereas U. aurantiacoatra forms a community with Andreaea spp.

Considering the knowledge accrued on successional patterns in this zone, a logical question that arises from the species list reported to be associated with the thalli of U. antarctica by M-M et al. (2013), is whether those species were already there before U. antarctica or vice versa. This is essential to understand the facilitation effect of U. antarctica which, as a facilitator, must have colonized the site before all the other species. However, considering the life history of several taxa, the interpretation of M-M et al. (2013) of the association between species is confusing at least. For instance, Ochyra (1998) and Ochyra et al. (2008) describe several mosses as pioneer species (Andreaea gainii Cardot, A. regularis Müll. Hal, and other Polytrichum spp.), as well as the lichen C. sublobulata in a recent monitoring of the primary succession of cryptogams after glacial recession on Signy Island (Favero-Longo et al. 2012). Thus, these species might have established before U. antarctica. In contrast, P. contortuplicata, Cladonia sp. and P. hypnorum appear at later successional stages. Sanionia uncinata (Hedw.) Loeske and Brachythecium austrosalebrosum (Müll.Hal.) Kindb. occur temporarily in early succession, and U. antarctica (and U. aurantiacoatra), R. geographicum and S. alpinum are multi-stage species, which appear contemporarily throughout the whole succession (Favero-Longo et al. 2012). In this sense, only the late-stage species could take advantage of the possible facilitation effects of well-developed lichen communities.

Survival of Deschampsia antarctica

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

The paper of M-M et al. (2013) attempted to determine ‘whether survival of seedlings of D. antarctica is increased when planted within cushions of U. antarctica compared to bare soil’. This attempt seems merely philosophical, considering that the authors did not find D. antarctica naturally growing within U. antarctica and that Antarctic phanerogams have not been observed to naturally associate with this lichen, nor are they abundant on bare soil; instead they typically thrive on cushions of several moss species, as has been reported by competent botanists and ecologists (Komárková et al. 1985; Ochyra 1998; Smith 2003). For example, Casanova-Katny & Cavieres (2012) showed that on ten different sites along the Antarctic Peninsula, D. antarctica grows positively associated with moss carpets dominated by Sanionia spp.; fruticose and crustose lichen communities tend to occur at the most xeric places, with strong winds, whereas D. antarctica usually grows associated with moss carpets, or on sites with a seasonal water supply (i.e. run-off from glacier ice or snow banks) and also occurs near abandoned penguin and bird nesting sites, on sandy mineral, well-drained substrates that do not have a continuous water supply throughout the season, but have some moisture-holding capacity (Komárková et al. 1985).

For the experiment, M-M et al. (2013) did not use recently germinated seedlings but adult plants, without explaining, however, their concept of an adult plant: do they refer to a tiller, with or without spikes, or to a tussock of defined size consisting of several tillers? The authors indicate only that the weight of the transplanted bulk of substrate was about 500 g, but do not mention from which substrate the plants were originally taken (i.e. bare soil or moss carpets; both are typical but contrasting habitats at the study site, as reported by Casanova-Katny & Cavieres 2012). The procedure for the transplantation experiments is also unclear: as the lichen thalli are supposed to grow on rocky ground, was the grass with the adhering 500 g of roots and soil placed directly on the lichens, between the stones or in rock crevices?

Finally, according to the paper, the transplant experiments were performed during 2010–2011, but survival of D. antarctica was only measured during 1 mo in 2010. It is not explained what happened in the second year: was the evaluation repeated or had the plants died? Our own transplant experiments conducted at Juan Carlos Point on the west coast of Fildes Peninsula showed no differences in survival after 1 yr between individual tillers transplanted within and outside moss carpets (Casanova-Katny & Cavieres 2012). In other transplant experiments, D. antarctica seedling survival was not affected after the first year, but decreased after 3 yrs to ca. 50% (Casanova-Katny, unpubl.). An adequate duration of this type of in situ experiment in the Antarctic (at least one full annual cycle) is crucial to obtain ecologically relevant responses. In conclusion, future studies should consider a more fully developed experimental design and avoid trying to demonstrate a spatial pattern that does not exist.

Micro-environment

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

With the purpose of characterizing the study site and to explain the possible mechanisms of facilitation by the lichen, M-M et al. (2013) measured several abiotic factors during a so-called ‘typical day’. However, there is no specification of what a ‘typical day’ means in the maritime Antarctic environment, where weather conditions can often change drastically and repeatedly over short intervals and even during the diurnal cycle. Indeed, the presented results are sharply different from those shown in reports from the same area and other adjacent localities (Kappen 1985; Casanova-Katny et al. 2010).

According to the authors, U. antarctica thalli ameliorate the microclimatic conditions beneath their canopies, considering soil nutrient content and matric potential as ‘microclimatic factors’ when actually being environmental factors. Soil moisture was measured as soil matric potential, which at the study sites is only feasible in deep soil accumulated in rock crevices. However, Antarctic lichens generally dominate in xeric habitats, avoiding sites with a constant water supply (Schlensog et al. 2003); also, as rootless organisms, lichens do not depend on soil for mineral or water uptake (Kappen 2000). M-M et al. (2013) indicate that matric potential values were obtained from soil beneath ‘large’ lichen cushions of 80–100 cm diam. at 10-cm depth, which probably refers to colonies consisting of several lichen thalli of both Usnea species.

Soil water potential between rocks was compared with the surrounding bare ground, which is composed of gravel and pebbles, as can be seen in the fig. 1 of M-M et al. (2013); measured values were between −15 and −22 KPa, with an increase of 6% under the lichen thalli. Nevertheless, both are values for well-hydrated soils, indicating that in biologically relevant terms there is no difference in soil moisture ‘beneath’ and ‘outside’ Usnea thalli. But more importantly, these measurements were taken at 10-cm depth, which is clearly not relevant for lichens that do not have roots and therefore cannot actively change soil water content. Although this environmental factor could be important for Deschampsia survival, it has to be recalled that the two organisms do not co-occur. What remains to be explained is how a ceramic cup tensiometer can be dug down to 10-cm depth within rocks, and how lichen thalli can increase soil water content to make the facilitation question feasible.

Moreover, M-M et al. (2013) indicated that substrate temperature, measured at 1 cm height above ground with an infrared thermometer (CHY-110), was ca. 1.2 °C higher in lichens than above bare ground. However, infrared thermometers measure the temperature of a surface but not the air surrounding that surface. Further, according to the manufacturer of the CHY-110 infrared thermometer, resolution and accuracy of this equipment are 0.5 °C (not 0.01 °C, as wrongly indicated in M-M et al. 2013) and ±2 °C, respectively. Thus, the temperature difference between the two microhabitats reported in M-M et al. (2013) falls within the error range of the equipment. Kappen (1985), when studying microclimatic factors affecting the lichen communities growing on rocks on Fildes Peninsula, King George Island (the same locality where the study of M-M et al. 2013 was carried out), found that when the air temperature reached values between 0 and 5 °C, both rock substrate and Usnea thalli temperatures were similar and slightly higher, reaching maximum values of ca. 10 °C.

In summary, the suggested nurse effect of the lichen thalli of U. antarctica on D. antarctica is of little or no relevance because the two species are not spatially associated in the maritime Antarctic, and the monitored period (1 mo) is clearly too short to predict a possible long-term association under a climate change scenario. In contrast to lichens, plant with roots are able to obtain moisture from deeper mineral layers. Lichens do not actively modify temperature, nor water availability or nutrient supply, and the taxa reported by M-M et al. (2013) clearly represent species-dependent substrate preferences, and suggest the necessity to first understand the primary succession of Antarctic fellfield species. Thus, it is not possible to compare the association of crustose or fruticose lichens growing on gravel with other species growing on moss or stones. Positive inter-specific interactions play a pivotal role in the structure and functioning of several ecosystems in harsh environments, and without doubt they must play a role in Antarctic terrestrial ecosystems. However, more rigorous and well-planned research is needed.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References

We would like to thank Dr. Seppelt and the anonymous reviewer for their valuable comments which have improved our manuscript. This work was supported by FONDECYT 1120895, FONDEF IDeA Ca 12i10224 and INACH FR0112.

References

  1. Top of page
  2. Abstract
  3. Studied species
  4. Association patterns
  5. Survival of Deschampsia antarctica
  6. Micro-environment
  7. Acknowledgements
  8. References
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