Temperate extension of the European range of Riccia crustata Trab.

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© 2014 J. Cramer in Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, www.borntraeger-cramer.deGermany. DOI: 10.1127/0029-5035/2014/0172 0029-5035/2014/0172 $ 2.00

Nova Hedwigia Vol. 98 (2014) Issue 3–4, 473–480 published online February 06, 2014; published in print May 2014

ArticleC

Temperate extension of the European range of Riccia crustata Trab.

Vincent Hugonnot1, Florine Pépin2 and Laurent Servière3

1 Pôle bryophyte, Conservatoire Botanique National du Massif Central, le Bourg, 43230 Chavaniac-Lafayette, France2 16, avenue des Gargailles 63 370 Lempdes, France3 Conservateur de la Réserve Naturelle Combe Lavaux – Jean Roland, Communauté de communes de Gevrey-Chambertin, 25 av. de la Gare – BP 34, 21220 Gevrey- Chambertin, France

With 3 figures and 1 table

Abstract: The rare liverwort Riccia crustata Trab. has been discovered in Burgundy (France), 350 km north of the nearest known locality. An updated map of the distribution in Europe, North Africa and Asia is provided. The plant communities are described and associated bryophytes are listed. Issues relating to conservation are discussed.

Key words: Riccia crustata, Burgundy, France, geographical distribution, grassland.

Introduction

Riccia crustata Trab. (Fig. 1) is a rare liverwort. It is mentioned as having a Vulnerable (VU) IUCN status in the Red Data Book of European Bryophytes (ECCB 1995). It is Critically endangered (CR) in Bulgaria (Natcheva et al. 2006). Its status in several countries remains obscure due to the scarcity of floristic data. The ecology of the species still remains badly known in the non Mediterranean areas due of the low number of records.

The world distribution of Riccia crustata is still unclear due to the uncertain status of the related Riccia albida Sull., which is considered doubtfully distinct (Schuster 1992, Jovet-Ast 2000). R. albida is confined to North America and Australia (Schuster 1992, Jovet-Ast 2000) whereas R. crustata (Fig. 2) is recorded from Europe, the Mediterranean bassin, central Asia (Ladyzhenskaia 1959) and Australia (Jovet-Ast 2000). R. crustata is recorded from the following countries in north Africa (Algeria, Egypt, Libya, Morocco, Tunisia) and Asia (Israel, Lebanon, Jordan, Kazakhstan)

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(Ladyzhenskaia 1959, Frey & Kürschner 1991, Bischler 2004, Heyn & Herrnstadt 2004, Ros et al. 2007, Kürschner & Frey 2011). A taxonomic reappraisal of the Riccia crustata complex is urgently needed on a worldwide basis. Considering the polymorphism of the species it is likely that more than two taxa are involved.

Riccia crustata is recorded from a few countries in Europe. Its known distribution extends to continental Spain and the Balearic Islands (Brugués et al. 2010), France (Offerhaus & Hugonnot 2004, Hugonnot 2010), Cyprus (Jovet-Ast 1986) and Bulgaria (Petrov 1966, Natcheva pers. comm.). It has been excluded from Portugal (Söderström et al. 2007) although it was mentioned in Bischler (2004). The species seems rather widespread and locally abundant in Spain where more than 20 populations are registered (Brugués et al. 2010), whereas it is very rare in France (only seven localities recorded) and Bulgaria (only two, Natcheva pers. comm.).

Fig. 1. Riccia crustata colony from Burgundy, showing sterile thallus.

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New chorological and ecological observations were made recently in France, most notably in Burgundy. In this paper it is intended to update the distribution of R. crustata in a worldwide context and to underline the ecological requirements of this species.

Nomenclature

Nomenclature of species according to Ros et al. (2007) for liverworts, Ros et al. (2013) for mosses and Kerguélen (1993) for vascular plants.

Results

New localities: Burgundy, Côte-d’Or, Gevrey-Chambertin, Réserve naturelle de la Combe Lavaux-Jean Rolland, 473 m a.s.l., 16 june 2013, 4°56'32,8"E; 47°13'33,1"N; V.Hugonnot & F.Pépin. Rhône-Alpes, Ardèche, Saint-Marcel-d’Ardèche, Pradinas, 200 m a.s.l., 3 june 2013, 4°35'18,8"E; 44°20'47,6"N; V.Hugonnot.

The newly discovered locality of Burgundy (France) is dominated by an insolated and dense calcareous grassland with Ranunculus gramineus, Valeriana tuberosa and Filipendula vulgaris of the Ranunculo graminei-Brometum erecti Royer 1973. Calcareous flat rock surfaces ("pavements") are colonized by the Poetum badensis Royer 1982 (Poa badensis, Sedum sp., Scilla automnalis). Two highly specialized vegetation assemblages are settled in shallow temporary ponds with a recurrent dry phase, the Allio schoenoprasi-Deschampsietum mediae de Laclos & Royer 2001 and the Junco

Fig. 2. Distribution of Riccia crustata in Europe, North Africa and Asia.

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sphaerocarpi-Lythretum hyssopifoliae de Laclos & Royer 2001 (Laclos & Royer 2001). Although no specific study aimed at understanding hydrological functioning of habitats is available, the length of the hydroperiod certainly demonstrates a great inter-annual or seasonal variability. Successive inundation periods are less than 24 hours in duration so that ponds are inundated less than one month a year. The size of the largest depressions is 50 m² and most of them are between 5 to 10 m².

The Allio schoenoprasi-Deschampsietum mediae is characterized by the co-occurrence and dominance of Allium schoenoprasum and Deschampsia media. It develops in shallow temporary ponds filled-in with calcareous silt (HCL+), on thin pavements devoid of cracks allowing the water to drain away immediately (Fig. 3).

The Junco sphaerocarpi-Lythretum hyssopifoliae is characterized by Juncus sphaero-carpus, Sisymbrella aspera and Centaurium pulchellum. It is settled in a comparable context.

The two types of vegetation and soils are strongly mutually associated with each other, the Allio schoenoprasi-Deschampsietum mediae being typical of soil more than 5 cm deep and the Junco sphaerocarpi-Lythretum hyssopifoliae of soils less than 5 cm deep, the latter being typical of more pronounced depressions in the ground.

Bryophytes frequently are intimately associated with one vegetation type (Fig. 3, Table 1). Riccia crustata is strongly linked to the Junco sphaerocarpi-Lythretum hyssopifoliae vegetation type and is very scarce in the Allio schoenoprasi-Deschampsietum mediae. Riccia sorocarpa and R. warnstorfii are also associated with the first association while R. gougetiana is more dessiccation tolerant, being linked to Allio schoenoprasi-Deschampsietum mediae. Acrocarp pioneer species dominate in the Allio schoenoprasi-Deschampsietum mediae while pleurocarps are dominant in the Ranunculo graminei-Brometum erecti.

In Ardèche (France), Riccia crustata shows very similar ecological requirements, being associated with Trichostomum crispulum, Didymodon acutus, Pleurochaete squarrosa,

Fig. 3. Section through the calcareous grassland mosaïc of Burgundy (Numbers refer to vegetation units in Table 1).

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Dicranella howei, Gymnotomum viridulum, Bryum dichotomum, Riccia bifurca, R. sorocarpa, and Barbula convoluta in small temporary ponds.

Discussion

Riccia crustata heretofore was confined to the Mediterranean region or the Great steppe region in Kazakhstan but its area is now extended towards the temperate climatic zone of France. The climate of the region where R. crustata was recently gathered corresponds to a xerothermic corridor that ranges from south Ardèche to the Dijon region. Its range is then extended 350 km north of the Ardèche localities. It is shown, therefore, that the species penetrates the European temperate climatic zone.

Bischler (2004) and Jovet-Ast (1986) summed up the ecological requirements of R. crustata in a Mediterranean context. It has been mentioned in arid and moist Mediterranean climates, in a wide variety of habitats, from grasslands, matorral to conifer forests, often in depressions with a pH of 7–8. In the Mediterranean area the species is mostly found on saline soils, including gypsum soils (Jovet-Ast 1973, Ros & Guerra 1987). In Spain (Casas 1970, 1973, 1975; Jovet-Ast 1973; Ros & Guerra 1987) it is strongly linked to saline soils of calcareous or gypsum land in the clearings of halophilous vegetation comprised of Suaeda fruticosa var. brevifolia and Frankenia pulverulenta. Ros & Guerra (1987) described a new alliance (Pottio commutatae-Riccion crustatae Ros & Guerra ex Marst 2006) to incorporate the bryophytic vegetation developped on saline soils with middle to high conductivity. Riccia crustata is a character species of the temporary hygrophilic Pottio pallidae-Riccietum crustatae Cano, Guerra & Ros 1997.

Table 1. Character bryophyte taxa of calcareous grassland associations in Burgundy (species are classified in a decreasing order of abundance).

Reference number 1 2 3 4

Vegetation type Junco sphaerocarpi-Lythretum hyssopifoliae

Allio schoenoprasi-Deschampsietum mediae

Ranunculo graminei-Brometum erecti

Buxus thicket

Floristic assemblage

Bryum alpinum Riccia crustata Riccia sorocarpa Riccia warnstorfii

Campyliadelphus elodes Bryum pseudo-triquetrum Fissidens adian-thoides Riccia gougetiana Weissia brachy-carpa Trichostomum crispulum Campyliadelphus chrysophyllus Barbula convoluta Didymodon acutus

Hypnum cupressifor-me var. lacunosum Pleurochaete squar-rosa Ctenidium mollus-cum Abietinella abietina var. hystricosa Ditrichum gracile Ceratodon purpureus subsp. purpureus

Rhytidiadelphus triquetrus Dicranum sco-parium Rhytidium rugo-sum

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The ecology of the localities in Alpes-Maritimes (France) was described in Offerhaus & Hugonnot (2004). There Riccia crustata is a typical inhabitant of temporary wet Deschampsia media grassland. In denudated patches this species is part of a species-rich Pottiaceous assemblage (with Trichostomum crispulum, Pleurochaete squarrosa, Tortella inclinata var. densa, Didymodon acutus, Aloina aloides, Campyliadelphus chrysophyllus, Encalypta vulgaris, Microbryum curvicollum, M. davallianum, Oxyrrhynchium hians and Polytrichum piliferum). It also inhabits a species-poor assemblage of bryophytes, mostly with Riccia bifurca Hoffm and Bryum alpinum With., in shallow and bare depressions.

The vegetation structure of the Burgundy site is remarkably similar to that of Alpes-Maritimes or Ardèche (France), with dominance of Riccia crustata in denudated and low-lying micro-ponds, rich Pottiaceous assemblages in grasslands and predominance of pleurocarps in Juniperus thickets (Offerhaus & Hugonnot 2004). If a slight physio-gnomic approach towards saline communities described in Spain is apparent, the ecological conditions appear strikingly distinct.

The bryophytic topographical sequence described in Burgundy appears original because it combines typical elements of mountain calcareous mires (Fissidens adianthoides, Campyliadelphus elodes, Bryum pseudotriquetrum) together with mediterranean xerothermic species like Trichostomum crispulum and Didymodon acutus, a fact, which is paralleled and epitomized by the occurence of Allium schoenoprasum, which is also a typical inhabitant of calcareous fens (Laclos & Royer 2001).

Conservation

The calcareous grasslands are generally managed as grazing land but this is not the case here. At the beginning of the dry period (June) water bodies may attract roe deers or boars that contribute significantly to localized erosion (Laclos & Royer 2001). Combined with oxidisation of accumulated organic matter during the dry phase, such habitats are likely to remain stable for a very long period of time. The antiquity of this vegetational mosaic has been previously suggested (Laclos & Royer 2001) and the disjunct occurence of Riccia crustata there adds further credance to this hypothesis.

Riccia crustata is a dioicous species and, as no sexual individuals are known in the Burgundy locality, sporophyte production is totally precluded. Regeneration of the thallus was obtained in R. crustata from dry specimens by Jovet-Ast (1973) and was also observed in the field in Burgundy, where small adventive thalli are formed at the margin of leading thalli. Hence, the maintenance of the species in that site relies strictly on vegetative multiplication through marginal budding so that it is difficult to see the Burgundy population as a recent arrival. R. crustata is most probably present there for a long time but has passed unnoticed due to its small size and low botanist appeal. A handfull of temporary ponds with Juncus spaerocarpus or Deschampsia media are known in Burgundy, in southern Jura or Chambaran plateau (France). They are mostly artificial sites which correspond to excavations, quarries or along paths and tracks. Significantly, recent surveys of these sites did not yelded any new populations

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of Riccia crustata even though ecological conditions appeared quite similar to those of natural stations.

Today, the Burgundy site benefit from statutory protection (Natural Reserve) and the biological value of calcareous temporary ponds have long been recognised by conservationists. Though very vulnerable to human activities, the site under consideration appears not directly threatened by anthropic impact. It is of great bryological interest because of the occurence of Riccia crustata and Campyliadelphus elodes (IUCN status RT, ECCB 1995), a suite of specialized taxa and a marked originality and ecological specialization of the vegetation.

The known populations of Ardèche or Alpes-Maritimes are accessible via 4×4 vehicles which constitute practically the only managment regime today because of generalized pasture abandonment. Though somehow paradoxical from a nature conservancy point of view, substrate compaction and erosion by motorized vehicles, provided this is not too frequent, is an efficient way to keep vegetational succession at an appropriate pioneer stage.

In Burgundy, this habitat remains, however, under non-negligible threat because of strong isolation from other population sources (Ardèche populations are 350 km south).

In the near future, climate change is likely to substantially affect the balanced hydrological regimes and limit the topographical extension of the more specialized vegetation types. A monitoring of the Burgundy population should be undertaken in the near future.

It would be of interest to make a conscious search for the species in comparable sites further north, in France or Germany, where comparable vegetation is recorded.

Acknowledgments

Thierry Vergne provided the map. Rayna Natcheva is warmly thanked for help with Bulgarian localities. Benoît Offerhaus’ help with French localities is gratefully aknowledged. Olivier Bardet offered valuable suggestions.

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Manuscript submitted August 30, 2013; accepted November 25, 2013.