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The response of the moss Campylopus lamellatus (Leucobryaceae Schimp.) post El Niño: a case study in the Caatinga

Abstract

Biological soil crusts (biocrusts) are important biological components in arid and semi-arid regions because they can serve as ecological facilitators for the vascular flora. Biocrusts of rocky outcrops of the Caatinga biome in the semiarid region of Northeast Brazil are comprised mainly of populations of the pioneer moss Campylopus lamellatus. Meanwhile, the Caatinga is undergoing progressive desertification, which is likely to continue for the next 100 years. Therefore, the physiological responses of C. lamellatus to climate change should be included in predictions regarding the future of the flora of these rocky environments. We evaluated a population of C. lamellatus during a prolonged drought brought about by El Niño, and during the first subsequent rainy season. We used biomass (dry mass) and proportion of chlorophyll as measures of tolerance. We identified decreased investment in biomass allocation and the degradation of photosynthetic pigments during the drought event. In contrast, we observed a rapid increase of chlorophyll during the rainy season, which represents biomass investment via chlorophyll regeneration. We conclude that the resilience of C. lamellatus is rapid, even for a photophilic plant, and should ensure its facilitative function under conditions of water saturation of the environment.

Key words:
Biomass; stress; photosynthesis; pigments; semiarid

Resumo

Biological soil crusts (biocrusts) são componentes importantes em regiões áridas e semiáridas, comumente associados à facilitação da flora vascular. Os biocrusts em afloramentos rochosos da Caatinga, no semiárido nordestino, são representados principalmente por populações do musgo pioneiro Campylopus lamellatus. Entretanto, a Caatinga está sob progressivo processo de desertificação, que deve se prolongar pelos próximos 100 anos. Assim, entender a resposta fisiológica de C. lamellatus sob um cenário de mudanças climáticas, deve basear previsões sobre o rumo da flora de ambientes rochosos em cenário futuro. Aqui, nós avaliamos uma população do musgo C. lamellatus durante o efeito prolongado de seca, causado pelo El Niño, e durante a primeira estação chuvosa após o fenômeno. Nós utilizamos a biomassa (massa seca) e proporção de clorofilas como medidas de vigor. Nós identificamos a diminuição do investimento em alocação de biomassa e a degradação dos pigmentos fotossintéticos durante o evento de seca. Em contrapartida, constatamos o rápido aumento das clorofilas durante a estação chuvosa, i.e., investimento em biomassa via regeneração de clorofilas. Desse modo, nós concluímos que a resiliência do C. lamellatus é rápida até mesmo para uma planta fotófila, o que deve assegurar sua função facilitadora em condições de saturação ambiental.

Palavras-chave:
Biomassa; estresse; fotossíntese; pigmentos; semiárido

The Caatinga is a Brazilian dry forest that is experiencing drastic desertification, with predictions of decreasing rainfall and increasing temperatures for at least the next 100 years (Vieira et al. 2015Vieira RMSP, Tomasella J, Alvalá RCS, Sestini MF, Affonso AG, Rodriguez DA, Barbosa AA, Cunha APMA, Valles GF, Crepani E, Oliveira SBP, Souza MSB, Calil PM, Carvalho MA, Valeriano DM, Campelo FCB & Santana MO (2015)Identifying áreas susceptible to desertification in the Brazilian Northeast. Solid Earth 6: 347-360.). This scenario should alter the distribution of species and, consequently, the dynamics of ecosystems. The rocky outcrops represent floral refuges with a wide variety of habitats (e.g., depressions, bare rock, cracks and soil islands) and diverse microclimates (Porembski et al. 1998Porembski S, Martinelli G, Ohlemuler R & Barthlott W (1998) Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest. Diversity and Distributions 4: 107-119.). They are unique environments with many endemic and rare Brazil plant species with limited distributions (Schneider & Boldrini 2012; Silva & Germano 2013Silva JB & Germano SR (2013) Bryophytes on rocky outcrops in the caatinga biome: a conservationist perspective. Acta Botanica Brasilica 27: 827-835.; Pereira et al. 2016Pereira JBS, Salino A, Arruda A & Stützel T (2016) Two new species of Isoetes (Isoetaceae) from northern Brazil. Phytotaxa 272: 141-148.; Silva et al. 2014Silva JB, Santos ND & Pôrto KC (2014) Beta-diversity: effect of geographical distance and environmental gradientes on the rocky outcrop bryophytes. Cryptogamie. Bryologie 35: 133-163.). Despite this, studies on the ecology of rocky outcrops are still incipient in Brazil (see Silva 2016Silva JB (2016) Panorama sobre a vegetação em afloramentos rochosos do Brasil. Oecologia Australis 20: 451-463.).

Bryophytes represent one of the most expressive components of biological soil crust in arid environments, such as rocky outcrops (Belnap & Lange 2001Belnap J & Lange OL (2001) Structure and functioning of biological soil crusts: a synthesis. In: Belnap J & Lange OL (eds.) Biological Soil Crusts: structure, function, and management. Springer-Verlag, Berlin. Pp. 471-479.). Biocrusts are associations between avascular organisms and soil particles, with the organisms living in or just above the ground (e.g., cyanobacteria, algae and bryophytes; Benalp & Lange 2001Belnap J & Lange OL (2001) Structure and functioning of biological soil crusts: a synthesis. In: Belnap J & Lange OL (eds.) Biological Soil Crusts: structure, function, and management. Springer-Verlag, Berlin. Pp. 471-479.). These associations can affect microclimates, facilitate germination, and alter nutritional status and survival of vascular plants (Benalp & Lange 2001Belnap J & Lange OL (2001) Structure and functioning of biological soil crusts: a synthesis. In: Belnap J & Lange OL (eds.) Biological Soil Crusts: structure, function, and management. Springer-Verlag, Berlin. Pp. 471-479.). These functions are especially important in arid and semi-arid regions and environments, such as the rocky outcrop ecosystems located in the dry forests of the Caatinga.

Among mosses common to biocrusts, Campylopus lamellatus Mont. (= Campylopus pilifer Brid. according Gama et al. 2017Gama R, Aguirre-Gutiérrez J & Stech M (2017) Ecological niche comparison and molecular phylogeny segregate the invasive moss species Campylopus introflexus (Leucobryaceae, Bryophyta) from its closest relatives. Ecology and Evolution 7: 8017-8031.) stands out as an abundant species on rocky outcrops (Silva et al. 2014Silva JB, Santos ND & Pôrto KC (2014) Beta-diversity: effect of geographical distance and environmental gradientes on the rocky outcrop bryophytes. Cryptogamie. Bryologie 35: 133-163., 2018Silva JB, Sfair JC, dos Santos ND & Pôrto KC (2018)Bryophyte richness of soil islands on rocky outcrops is not driven by island size or habitat heterogeneity. Acta Botanica Brasilica 32: 161-168.; Penãloza-Bojacá et al. 2018Peñaloza-Bojacá GF, Oliveira BA, Araújo CAT, Fantacelle LB, dos Santos ND & Maciel-Silva AS (2018) Bryophytes on Brazilian ironstone outcrops: diversity, environmental filtering, and conservation implications. Flora 238: 162-174. DOI 10.1016/j.flora.2017.06.012
https://doi.org/10.1016/j.flora.2017.06....
). It is an acrocarpic pioneer moss of rocky outcrops (Oosting & Hess 1956Oosting HJ & Hess DW (1956) Microclimate and a relic stand of Tsuga Canadensis in the Lower Piedmont of North Carolina. Ecology 37: 28-39.; Scarano 2002Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rain forest. Annals of Botany 90: 517-524.), and is widely distributed worldwide. In the Neotropics the species occurs at high elevations, reaching up to 3500 m (Gradstein & Sipman 1978Gradstein SR & Sipman HJM (1978) Taxonomy and world distribution of Campylopus introflexus and C. lamellatus (= C. polytrichoides): a new synthesis. Bryologist 81: 11-121.). According to Gradstein & Sipman (1978)Gradstein SR & Sipman HJM (1978) Taxonomy and world distribution of Campylopus introflexus and C. lamellatus (= C. polytrichoides): a new synthesis. Bryologist 81: 11-121., the species requires a humid climate, at least periodically, for population persistence. It is recognized as being adapted to xeric climates, possessing morpho-anatomical attributes that allow it to colonize and persist therein. Such attributes include well-developed and internally-differentiated strands arranged in stereochemical bands that decrease mechanical stress during desiccation events (Frahm 1990Frahm J-P (1990) Bryophyte phytomass in tropical ecosystems. Botanical Journal of the Linnean Society 104: 23-33.). Its costa, occupying more than two-thirds of the width of the leaves, is the main site for photosynthesis, and acts in gas exchange and effective water conduction (Frahm 1985Frahm J-P (1985) The ecological significance of the costal anatomy in the genus Campylopus. Abstracta Botanica 9: 159-169., 1990Frahm J-P (1990) Bryophyte phytomass in tropical ecosystems. Botanical Journal of the Linnean Society 104: 23-33.). Its tall lamellae allow the photosynthetically active period to be extended in dry environments (Frahm 1985Frahm J-P (1985) The ecological significance of the costal anatomy in the genus Campylopus. Abstracta Botanica 9: 159-169.). Thus, understanding the responses of C. lamellatus to climate change can facilitate predictions regarding the flora of dry environments and allow inferences to be made regarding the dynamics of plant communities.

Catimbau Valley National Park (PARNA Catimbau; 08º24’-08º36’S × 37º09’-37º14’W), possesses a horizontal gradient of rainfall with extremes differing by 500 mm (Rito et al. 2017Rito KF, Arroyo-Rodríguez V, Queiroz RT, Leal IR & Tabarelli M (2017) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. Journal of Ecology 105: 1-10.). Considering the effects of climatic change on the Caatinga (Vieira et al. 2015Vieira RMSP, Tomasella J, Alvalá RCS, Sestini MF, Affonso AG, Rodriguez DA, Barbosa AA, Cunha APMA, Valles GF, Crepani E, Oliveira SBP, Souza MSB, Calil PM, Carvalho MA, Valeriano DM, Campelo FCB & Santana MO (2015)Identifying áreas susceptible to desertification in the Brazilian Northeast. Solid Earth 6: 347-360.), changes in the spatial distribution of plant species are expected, particularly so for bryophytes, which should accompany the moisture gradient and move towards more humid extremes (Tng et al. 2009Tng DYP, Danton PJ & Jordan GJ (2009) Does moisture affect the partitioning of bryophytes between terrestrial and epiphytic substrates within cool temperate rain forests? The Bryologist 112: 506-519.; Sun et al. 2013Sun S-Q, Wu Y-H, Wang G-X, Yu D, Bing H-J & Luo J (2013) Bryophyte species richness and composition along an altitudinal gradient in Gongga Mountain, China. PLoS One 8: e58131.). This pattern should be intensified by the broad geographic distribution of many bryophyte species (i.e., long-distance dispersion via spores), with shifts in the distribution of plants according to the rate of the climate change. New records for bryophyte species have come from some very unlikely locations [e.g., Crossidium crassinerve (De Not.) Jur., Dicranella howei Ren. et Card., Frullania inflata Gottsche - Pócs (2011)Pócs T (2011) Signs of climate changes in the bryoflora of Hungary. In: Tuba Z, Slack NG & Stark LR (eds.) Bryophyte ecology and climate change. Cambridge University Press, London. Pp. 359-370.]. Although it is difficult to pinpoint the causes of changes in the distributions of bryophytes (see Frahm & Klaus 2000Frahm J-P & Klaus D (2000) Moose als Indikatoren von rezenten und früheren Klimafluktuationen in Mitteleuropa. NNA-Berichte 2/ 2000: 69-75.; Kürschner 2002Kürschner H (2002) Life strategies of Pannonian loess cliff bryophyte communities. Studies on the cryptogamic vegetation of loess cliffs, VIII. Nova Hedwigia 75: 307-318.), Pócs (2011)Pócs T (2011) Signs of climate changes in the bryoflora of Hungary. In: Tuba Z, Slack NG & Stark LR (eds.) Bryophyte ecology and climate change. Cambridge University Press, London. Pp. 359-370. suggests that at least some of these records are potentially due to the influence of climatic change.

We collected two 10 × 10 cm samples of C. lamellatus from the same population (approximately 1 m2): one in July 2016 during drought season (El Niño effect) and one during the first rainy season post El Niño in June 2017. In July of 2016, the mean daily rainfall for the month was approximately 0.93 mm, with rain concentrated in only two days, while the mean monthly temperature was 22.9 °C. The El Niño event of 2015-16 exhibited relatively high anomalies and had major impacts on the dynamics and structure of the tropical ecosystems worldwide (Brito et al. 2017Brito SSB, Cunha APMA, Cunningham CC, Alvalá RC, Marengo JA & Carvalho MA (2017) Frequency, duration and severity of drought in the Semiarid Northeast Brazil region. International Journal of Climatology 23: 200-213.). In Brazil, this event caused an extreme dry climate in the semiarid region. In June 2017, the mean daily rainfall for the month was approximately 3 mm, with rains on every day, while the mean monthly temperature was 19.4 °C (National Institute of Meteorology INMET <http://www.inmet.gov.br>). The response of the moss population to the differing climates of the two periods was evaluated using variation in dry mass and pigment parameters [i.e., amounts of chlorophyll a (Chl a) and chlorophyll b (Chl b) and the proportion chlorophyll a:chlorophyll b (Chl a:b)], according to Marschall & Proctor (2004)Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.. We packed the samples in ziplock bags to conserve moisture and they were maintained in the dark at 10 ºC.

We measured the mass of 50 gametophytes for each climatic period on a precision scale (0.0001 g). We then dried the samples at 80 °C for 72 h, and then reweighed them to obtain dry mass (adapted from Marschall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.), which we treat as biomass here. For the pigment parameters, we macerated 100 mg of botanical material in a darkened environment and added 10 ml of 80% acetone. The solution was allowed to settle for 24 h in the dark in a test tube enveloped with paper and foil for the complete separation of possible substrate particles and for measuring the amount of pigments (Lichtenthaler 1987Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382.). The amounts of the photosynthetic pigments Chl a and Chl b were measured (in triplicate) using a spectrophotometer at absorbances of 645 and 663 nm, respectively (Lorenzen 1967Lorenzen CJ (1967) Determination of chlorophyll and phaeo-pigments spectrophotometric equations. Limnology and Oceanography12: 343-346.; Peñuela 1984Peñuela J (1984) Pigment and morfological response to emersion and immersion of some aquatic and terrestrial mosses in NE spain. Journal of Bryology 13:179-185.; Martínez & Sánchez 1987; Marschall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.). We removed the acetone effect by calculating the difference between the pigment solution and the acetone content by reading the pure acetone at each absorbance. We transformed the results using the following typical equations in bryophyte’s physiology: Ca = 12.3 * E663 - 0.86 * E645; Cb = 19.3 * E645 - 3.6 * E663; Ca + Cb = 8.7 * E663 + 18.4 * E645, where Ca and Cb indicate the concentrations of chlorophyll a and b, respectively. Since these results are in mg/L, we converted them to mg/g wet weight by the following equation: C = (Ca * V)/g, where Ca indicates the value for ​​chlorophyll a in mg/L; V indicates the volume of the extraction in L; and g indicates the weight of the moss sample (G.M. Gecheva - personal communication).

Biomass (mean ± SD: dry = 14.04 mg ± 8.48 mg, rainy = 16.70 mg ± 9.80 mg) did not vary significantly between sampling periods (t-student test, t = -1.453, n.s.). This can be explained by the lack of adequate weather and climate for investment in growth between the end of the drought season and the next sampling period (subsequent rainy season) about six months later. Nonetheless, biomass increased slightly in the rainy season, which may be indicative of initial investment in the accumulation of dry mass by gametophytes.

Chlorophyll a levels were generally higher in the rainy season (Mann-Whitney test: Z = -1.963, P = 0.049), but there was no significant difference in chlorophyll b levels (Z = -1.385; n.s.) or in the chl a:b ratio (Z = -0.654; n.s.). It should be noted that Chl a levels increased by a factor of four times during the rainy season and that Chl b levels also increased during the rainy season, but not significantly so (Table 1). Although the pigment levels ​​are considered normal for species of bryophytes adapted to xeric environments (Martín & Churchill 1982Martin CE & Churchill SP (1982) Chlorophyll concentrations and a/b ratios in mosses collected from exposed and shaded habitats in Kansas. Journal of Bryology 12: 297-304.; Marshall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.), the increase of chlorophyll levels in the rainy season shows that variation in rainfall is a determinant for the development of the bryophytes (Ueno et al. 2006). On the other hand, the non-significant difference in chlorophyll b levels and chl a:b between the two climatic extremes indicates investment in protective processes, such as photoinhibition, as has been documented for Campylopus introflexus, another species of the genus (García et al. 2016Garciá EL, Rosenstiel TN, Graves C, Shortlidge EE & Eppley SM (2016) Distribution drivers and physiological responses in geothermal bryophyte communities. American Journal of Botany 103: 625-634.).

Chlorophyll degradation is a well-known process. One of the elementary factors for triggering this process is environmental stress, such as prolonged drought (Hendry et al. 1987Hendry GAF, Houghton JD & Brown SB (1987) The degradation of chlorophyll - a biological enigma. New Phytologist 107: 255-302.). The increase in chlorophyll content in C. lamellatus may be linked to decreased available sunlight during the rainy season (due to increased cloudiness) and to increased biomass of gametophytes. The investment in biomass must be accompanied by increased leaf production, which thereby increases the concentration of chlorophyll. This explanation is consistent with the data presented by Carvalho et al. (2007)Carvalho APF, Bustamante MMC, Kozovits AR & Asner GP (2007) Variações sazonais nas concentrações de pigmentos e nutrientes em folhas de espécies de cerrado com diferentes estratégias fenológicas. Revista Brasileira de Botânica [Brazilian Journal of Botany] 30: 19-27. for vascular plants of open and closed Cerrado. Although there are differences in the concentrations ​​of chlorophyll molecules between vascular and avascular plant groups, there is also great overlap (Marschall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.). This is explained by the fact that increased or decreased concentrations vary according to the level of solar radiation, for example (Marschall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.).

The proportion of chlorophylls a:b (1.65, s.d. ± 1.13) of this species in the dry season is much lower than that found for other species in exposed environments (2.51, s.d. = 0.22 - Martín & Churchill (1982)Martin CE & Churchill SP (1982) Chlorophyll concentrations and a/b ratios in mosses collected from exposed and shaded habitats in Kansas. Journal of Bryology 12: 297-304.; 2.39, s.d. = 0.51 - Marschall & Proctor 2004Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.). This indicates that the level of solar radiation experienced in dry seasons in the Caatinga in rocky outcrops is particularly higher than in the surrounding matrix. Campylopus lamellatus presents Type 3 light curves (Bates et al. 2009Bates JW, Wibbelmann MH & Proctor MCF (2009)Salinity responses of halophytic and non-halophytic bryophytes determined by chlorophyll fluorometry. Journal of Bryology 31: 11-19.), which indicates a photoprotective response to light intensities above normal including maintaining the trans-thylakoid pH gradient necessary for zeaxanthin-PSBS-mediated quenching (Gerotto et al. 2012Gerotto C, Alboresi A, Giacometti GM, Bassi R & Morosinotto T (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytologist 196: 763-73.; Proctor & Smirnoff 2015Proctor MCF & Smirnoff N (2015) Photoprotection in bryophytes: rate and extent of dark-relaxation of non-photochemical quenching (NPQ) of chlorophyll fluorescence. Journal of Bryology 37: 171-177.; Proctor & Bates 2018Proctor MCF & Bates JW (2018) Chlorophyll-fluorescence measurements in bryophytes: evidence for three main types of light-curve response. Journal of Bryology 40: 1-11.).

Bryophytes cushion susceptibility to erosion and aid in the uptake and retention of nutrients, and thus affect the structure of vascular plant communities (Belnap & Weber 2013Belnap J & Weber B (2013) Biological soil crusts as an integral component of desert environments. Ecological Processes 2: 11.). These plants constitute one of the least studied plant groups in xeric environments, especially in the case of rocky outcrop ecosystems (see Silva 2016Silva JB (2016) Panorama sobre a vegetação em afloramentos rochosos do Brasil. Oecologia Australis 20: 451-463.). Because they are poikilohydric, conditions of high aridity may hinder establishment. Although the growth rates of bryophytes in dry environments are low when compared to those in mesic environments, their contribution to these ecosystems (e.g., structuring of sandy soils, and biomass accumulation) at the global level is of fundamental importance (Stark et al. 2011Stark LR, Brinda JC & McLetchie DN(2011) Effects of increased summer precipitation and N deposition on Mojave Desert populations of the biological crust moss Syntrichia caninervis. Journal of Arid Environments 75: 457-463.). We report a significant increase in chlorophyll a levels during the rainy season in a pioneering moss from a fragile Caatinga ecosystem. We suggest that during the rainy season, when there is greater water accumulation in the gametophytes due to poikilohydrism, the productivity of the population increases, which produces a discrete increase in biomass in a few months. A reduction in rainfall intensity or an increase in the duration of the rainy season, either due to climatic events such as El Niño or to global climatic changes, may alter the physiology of the studied species of moss, which may have drastic consequences for the dynamics and vegetation associated with rocky outcrops.

Acknowledgment

This research was supported by the Foundation for Science and Technology Support of the State of Pernambuco (FACEPE, process 1707-2.03/13) in the form of the first author’s doctoral scholarship. We are grateful to the Catimbau PELD for logistical support; to SISBio for granting permission to collect botanical material (authorization number 45504). The State University of Paraíba provided us with infrastructure to set up and follow up the experiment and analyses the data through the Plant Physiology and Aquatic Laboratories.

References

  • Bates JW, Wibbelmann MH & Proctor MCF (2009)Salinity responses of halophytic and non-halophytic bryophytes determined by chlorophyll fluorometry. Journal of Bryology 31: 11-19.
  • Belnap J & Lange OL (2001) Structure and functioning of biological soil crusts: a synthesis. In: Belnap J & Lange OL (eds.) Biological Soil Crusts: structure, function, and management. Springer-Verlag, Berlin. Pp. 471-479.
  • Belnap J & Weber B (2013) Biological soil crusts as an integral component of desert environments. Ecological Processes 2: 11.
  • Brito SSB, Cunha APMA, Cunningham CC, Alvalá RC, Marengo JA & Carvalho MA (2017) Frequency, duration and severity of drought in the Semiarid Northeast Brazil region. International Journal of Climatology 23: 200-213.
  • Carvalho APF, Bustamante MMC, Kozovits AR & Asner GP (2007) Variações sazonais nas concentrações de pigmentos e nutrientes em folhas de espécies de cerrado com diferentes estratégias fenológicas. Revista Brasileira de Botânica [Brazilian Journal of Botany] 30: 19-27.
  • Frahm J-P & Klaus D (2000) Moose als Indikatoren von rezenten und früheren Klimafluktuationen in Mitteleuropa. NNA-Berichte 2/ 2000: 69-75.
  • Frahm J-P (1985) The ecological significance of the costal anatomy in the genus Campylopus. Abstracta Botanica 9: 159-169.
  • Frahm J-P (1990) Bryophyte phytomass in tropical ecosystems. Botanical Journal of the Linnean Society 104: 23-33.
  • Gama R, Aguirre-Gutiérrez J & Stech M (2017) Ecological niche comparison and molecular phylogeny segregate the invasive moss species Campylopus introflexus (Leucobryaceae, Bryophyta) from its closest relatives. Ecology and Evolution 7: 8017-8031.
  • Garciá EL, Rosenstiel TN, Graves C, Shortlidge EE & Eppley SM (2016) Distribution drivers and physiological responses in geothermal bryophyte communities. American Journal of Botany 103: 625-634.
  • Gerotto C, Alboresi A, Giacometti GM, Bassi R & Morosinotto T (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytologist 196: 763-73.
  • Gradstein SR & Sipman HJM (1978) Taxonomy and world distribution of Campylopus introflexus and C. lamellatus (= C. polytrichoides): a new synthesis. Bryologist 81: 11-121.
  • Hendry GAF, Houghton JD & Brown SB (1987) The degradation of chlorophyll - a biological enigma. New Phytologist 107: 255-302.
  • Kürschner H (2002) Life strategies of Pannonian loess cliff bryophyte communities. Studies on the cryptogamic vegetation of loess cliffs, VIII. Nova Hedwigia 75: 307-318.
  • Lichtenthaler HK (1987) Chlorophylls and carotenoids pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382.
  • Lorenzen CJ (1967) Determination of chlorophyll and phaeo-pigments spectrophotometric equations. Limnology and Oceanography12: 343-346.
  • Marschall M & Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany 94: 593-603.
  • Martin CE & Churchill SP (1982) Chlorophyll concentrations and a/b ratios in mosses collected from exposed and shaded habitats in Kansas. Journal of Bryology 12: 297-304.
  • Oosting HJ & Hess DW (1956) Microclimate and a relic stand of Tsuga Canadensis in the Lower Piedmont of North Carolina. Ecology 37: 28-39.
  • Peñaloza-Bojacá GF, Oliveira BA, Araújo CAT, Fantacelle LB, dos Santos ND & Maciel-Silva AS (2018) Bryophytes on Brazilian ironstone outcrops: diversity, environmental filtering, and conservation implications. Flora 238: 162-174. DOI 10.1016/j.flora.2017.06.012
    » https://doi.org/10.1016/j.flora.2017.06.012
  • Peñuela J (1984) Pigment and morfological response to emersion and immersion of some aquatic and terrestrial mosses in NE spain. Journal of Bryology 13:179-185.
  • Pereira JBS, Salino A, Arruda A & Stützel T (2016) Two new species of Isoetes (Isoetaceae) from northern Brazil. Phytotaxa 272: 141-148.
  • Pócs T (2011) Signs of climate changes in the bryoflora of Hungary. In: Tuba Z, Slack NG & Stark LR (eds.) Bryophyte ecology and climate change. Cambridge University Press, London. Pp. 359-370.
  • Porembski S, Martinelli G, Ohlemuler R & Barthlott W (1998) Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest. Diversity and Distributions 4: 107-119.
  • Proctor MCF & Bates JW (2018) Chlorophyll-fluorescence measurements in bryophytes: evidence for three main types of light-curve response. Journal of Bryology 40: 1-11.
  • Proctor MCF & Smirnoff N (2015) Photoprotection in bryophytes: rate and extent of dark-relaxation of non-photochemical quenching (NPQ) of chlorophyll fluorescence. Journal of Bryology 37: 171-177.
  • Rito KF, Arroyo-Rodríguez V, Queiroz RT, Leal IR & Tabarelli M (2017) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. Journal of Ecology 105: 1-10.
  • Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rain forest. Annals of Botany 90: 517-524.
  • Silva JB & Germano SR (2013) Bryophytes on rocky outcrops in the caatinga biome: a conservationist perspective. Acta Botanica Brasilica 27: 827-835.
  • Silva JB (2016) Panorama sobre a vegetação em afloramentos rochosos do Brasil. Oecologia Australis 20: 451-463.
  • Silva JB, Santos ND & Pôrto KC (2014) Beta-diversity: effect of geographical distance and environmental gradientes on the rocky outcrop bryophytes. Cryptogamie. Bryologie 35: 133-163.
  • Silva JB, Sfair JC, dos Santos ND & Pôrto KC (2018)Bryophyte richness of soil islands on rocky outcrops is not driven by island size or habitat heterogeneity. Acta Botanica Brasilica 32: 161-168.
  • Stark LR, Brinda JC & McLetchie DN(2011) Effects of increased summer precipitation and N deposition on Mojave Desert populations of the biological crust moss Syntrichia caninervis. Journal of Arid Environments 75: 457-463.
  • Sun S-Q, Wu Y-H, Wang G-X, Yu D, Bing H-J & Luo J (2013) Bryophyte species richness and composition along an altitudinal gradient in Gongga Mountain, China. PLoS One 8: e58131.
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Edited by

Editor de área: Dr. Marcelo Mielke

Publication Dates

  • Publication in this collection
    23 Nov 2020
  • Date of issue
    2020

History

  • Received
    06 Feb 2019
  • Accepted
    02 June 2019
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