The Habitat of the Neglected Independent Protonemal Stage of Buxbaumia Viridis
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plants Article The Habitat of the Neglected Independent Protonemal Stage of Buxbaumia viridis Ameline Guillet 1, Vincent Hugonnot 2,* and Florine Pépin 2 1 Independent Researcher, 58 rue Georges Rissler, FR-63000 Clermont-Ferrand, France; [email protected] 2 Independent Researchers, Le Bourg, FR-43380 Blassac, France; fl[email protected] * Correspondence: [email protected] Abstract: Buxbaumia viridis is a well-known species of decaying deadwood, which is protected in Europe. All previous studies dealing with the ecology of B. viridis rely on the sporophyte generation because the gametophyte generation is allegedly undetectable. Recent advances have shown that the protonemal stage, including gemmae, is recognizable in the field, thereby considerably modifying our perception of the species’ range and habitat. In France, we demonstrate the existence of independent protonemal populations, with the implication that the range of B. viridis is widely underestimated. Sporophytes and sterile protonema do not share the same ecological requirements. The sporophyte stage was found in montane zones, almost exclusively in coniferous forests, and on well-decayed wood. The sterile protonemal stage extends to lower elevations, in broad-leaved forests, and on wood in a less advanced state of decay. Our results suggest that the humidity could be one of the most relevant explanatory variables for the occurrence of sporophytes. Opening of the canopy seems to promote sporophyte development. Previous anomalous observations of B. viridis growing on humus or bark might be explained by the presence of a protonemal population that is able to produce sporophytes under rarely occurring but favorable climatic events. Keywords: gemmae; decaying wood; dead-wood; ecological modelling; conservation Citation: Guillet, A.; Hugonnot, V.; Pépin, F. The Habitat of the Neglected Independent Protonemal Stage of 1. Introduction Buxbaumia viridis. Plants 2021, 10, 83. https://doi.org/10.3390/plants Buxbaumia viridis (Moug. ex Lam. et DC.) Brid. ex Moug. et Nestl. (Buxbaumiaceae) is 10010083 a hygrophilous, sciaphilous, and acidophilous species, widely distributed in the Northern hemisphere, where it mainly colonizes decaying wood in wet, shaded coniferous montane Received: 15 November 2020 woodlands [1–3]. Ecological factors, that have been suggested as relevant in explaining the Accepted: 27 December 2020 occurrence of the species, are the amount of available deadwood, the degree of its decom- Published: 2 January 2021 position, canopy openness, humidity, elevation, aspect, and deadwood composition [3–5]. As a species apparently linked to well-preserved forest stands with large accumulations Publisher’s Note: MDPI stays neu- of bulky woody debris, it has been suggested that B. viridis is an indicator of ancient tral with regard to jurisdictional clai- woodland [5]. ms in published maps and institutio- B. viridis is protected in Europe by Annex I of the Bern Convention [6], and Annex nal affiliations. II of the “Habitats-Fauna-Flora” Directive (Habitat Directive 92/43/EEC), since a large proportion of its habitat has disappeared worldwide during the 20th century [7]. Over recent decades the species has been assessed in the European Red-list for bryophytes as “vulnerable”, and this has led to a disproportionate increase in the number of targeted stud- Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. ies [3,4,8,9]. Hence its status has changed to “least concern” in the most recent Red-List [10]. This article is an open access article However, its conservation remains a matter of critical concern, for instance on account of distributed under the terms and con- forest management practices that lead to a reduction in coarse wood debris (CWD), or to ditions of the Creative Commons At- clear-felling which permits light penetration and consequently drought [11,12]. tribution (CC BY) license (https:// Unlike other mosses whose haploid gametophyte is dominant and clearly visible, creativecommons.org/licenses/by/ B. viridis possesses a minute gametophyte which consists of a filamentous protonema 4.0/). that produces much reduced female and male buds [4,13]. The distinctive protonema Plants 2021, 10, 83. https://doi.org/10.3390/plants10010083 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 14 Plants 2021, 10, 83 2 of 14 produces much reduced female and male buds [4,13]. The distinctive protonema has been previously described in vitro [14]. It comprises colorless, occasionally branched rhizoids, 15has μm been in diameter previously with described oblique incross-walls, vitro [14]. an Itd comprises an upright, colorless, somewhat occasionally undulating branched chloro- nematalrhizoids, filament 15 µm in system diameter with with relatively oblique frequent cross-walls, anastomosis and an upright, [13,14]. somewhat By contrast, undulating the spo- rophytechloronematal is disproportionately filament system large with and relatively can be from frequent 7 to 25 anastomosis mm long [3]. [13 ,14]. By contrast, the sporophyteBecause the is minute disproportionately gametophyte large of B. and viridis can is be reputedly from 7 to impossible 25 mm long to [3 spot]. in the field, Becauseall previous the minutestudies gametophytehave been based of B. on viridis the sporophyteis reputedly stage impossible [3–5]. However, to spot in one the recentfield, allstudy previous has described studies haveprotonemal been based gemmae on the (i.e., sporophyte asexual propagules) stage [3–5 ].in However, B. viridis [13]. one Theserecent gemmae study has are described multicellular, protonemal obloid, gemmae with a warty (i.e., asexualornamentation, propagules) and their in B. size viridis varies[13]. betweenThese gemmae 40 μm areand multicellular, 70 μm. They obloid,tend to with form a brownish, warty ornamentation, large and highly and their distinctive size varies ag- gregationsbetween 40 thatµm are and relatively 70 µm. easy They to tendlocate to in form the field brownish, (see Material large andand highlyMethods distinctive section). aggregationsBy conducting that are non-systematic relatively easy searches to locate all in over the fieldFrance, (see far Material beyond and the Methods current knownsection). range of the sporophytes of B. viridis, the authors were able to find many unex- pectedBy protonemal conducting populations, non-systematic for searchesinstance allin overthe Northern France, far Oceanic beyond and the Mediterranean current known regionsrange of of theFrance. sporophytes This led the of B.authors viridis to, thesuspect authors that werethe species able tocould find be many well-established unexpected atprotonemal numerous populations, sites far removed for instance from localiti in thees Northern where the Oceanic sporophytes and Mediterranean are known, regionsas pre- viouslyof France. suggested This led [14]. the authors to suspect that the species could be well-established at numerousIn this sites paper, far removedwe investigate from localities the vertical where distribution the sporophytes of both are stages known, of as B. previously viridis in Francesuggested (i.e., [ 14sterile]. protonema + sporophyte), and we study the ecology of the protonemal stage Infrom this a paper,conservation we investigate perspective. the Do vertical the protonema distribution and of sporophyte both stages share of B. the viridis samein ecologicalFrance (i.e., requirements sterile protonema at two + different sporophyte), scales, and namely we study habitat the ecology(forest stand) of the protonemaland micro- habitatstage from (decaying a conservation deadwood)? perspective. Do the protonema and sporophyte share the same ecological requirements at two different scales, namely habitat (forest stand) and 2.microhabitat Results (decaying deadwood)? 2.1.2. Results Distribution of Buxbaumia viridis 2.1. DistributionBuxbaumia viridis of Buxbaumia was found viridis in 79 forests spread over the 12 French departments (Fig- ure 1).Buxbaumia In 50 of them viridis thewas protonemal found in stage 79 forests was found. spread Sporophyte over the 12 stage French was departments found in 29 of(Figure them,1 ).which In 50 was of them always the accompanied protonemal stage by gemmae. was found. Sporophyte stage was found in 29 of them, which was always accompanied by gemmae. Figure 1. All 137 habitats (forest stands) surveyed. Black lines: French departments limits. © Google Terrain. Plants 2021, 10, 83 3 of 14 2.2. Habitat Definition of habitat is given in Materials and Methods section. The altitudinal distribution of the protonema localities ranged from 421 m to 1452 m a.s.l (Table1a). Sporophytes were observed at elevations between 840 and 1452 m a.s.l. More than half of the protonema localities were on north- (27%), northeast- (16%) or northwest-facing (10%) slopes. Of coniferous forests 74, of mixed 78, and of broad-leaved forests 15% contained B. viridis (Table1b). Only protonemal colonies were found in broad-leaved forests. Coniferous forests were dominated by Pseudotsuga menziesii, Abies alba or Picea abies. Mixed forests often consisted of Fagus sylvatica associated with P. menziesii or P. abies. Broad-leaved forests were dominated by F. sylvatica or Acer platanoides. Table 1. Description of the set of environmental quantitative variables (a) and qualitative variable (b) of all stands surveyed (137), stands containing Buxbaumia viridis (sporophyte + sterile protonema) (79) and stands containing sporophytes (29). No: number. (a)