Bryophyte taxonomic and functional groups as

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/257592824

Bryophyte taxonomic and functional groups as indicators of fine scale ecological gradients in mountain streams Article in Ecological Indicators · July 2012 DOI: 10.1016/j.ecolind.2011.10.012

CITATIONS

READS

16

270

4 authors: Cristiana Vieira

Ana Séneca

University of Porto

University of Porto

99 PUBLICATIONS 309 CITATIONS

42 PUBLICATIONS 326 CITATIONS

SEE PROFILE

SEE PROFILE

Cecília Sérgio

Maria Teresa Ferreira

University of Lisbon

University of Lisbon

197 PUBLICATIONS 1,763 CITATIONS

445 PUBLICATIONS 4,077 CITATIONS

SEE PROFILE

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Ferns of the Pacific View project

Managing Aquatic Ecosystems and Water Resources under Multiple Stress View project

All content following this page was uploaded by Cristiana Vieira on 21 January 2014.

The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately.

Ecological Indicators 18 (2012) 98–107

Contents lists available at SciVerse ScienceDirect

Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind

Bryophyte taxonomic and functional groups as indicators of fine scale ecological gradients in mountain streams C. Vieira a,∗ , A. Séneca b,c,d , C. Sérgio e , M.T. Ferreira f a

Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO - Research Centre in Biodiversity and Genetic Resources), Rua Do Campo Alegre, S/N, Edifício FC4, Sala 1.29, 4169-007, Portugal b Centro de Investigação em Biodiversidade e RecursosGenéticos (CIBIO - Research Centre in Biodiversity and Genetic Resources), Portugal c Department of Biology, Science Faculty of Oporto University, Portugal d Department of Biology, Norwegian University for Science and Technology, NTNU, Trondheim, Norway e National Museum of Natural History, Botanic Garden and Centre for Environmental Biology (CBA), Lisbon University, Lisbon, Portugal f Forest Research Centre, Technical University of Lisbon, Lisbon, Portugal

a r t i c l e

i n f o

Article history: Received 26 July 2011 Received in revised form 25 October 2011 Accepted 27 October 2011 Keywords: Bryophyte Watercourse Life form Life strategy Taxonomic group Flow velocity Light incidence Hydrologic zone Monitoring

a b s t r a c t Mountain stream monitoring is closely related to the survey of bryophyte species since it is there that these organisms are common and show very specialized ecological niches. This work hypothesizes that a close relationship between bryophyte taxonomic and functional categories and microhabitat conditions exists and proposes to explore this link as a basis for fine-scale monitoring. The distribution of bryophytes in mountain fluvial microhabitats of northwest and centre-west Portugal was examined at 165 locations. The response of higher level taxonomic groups and life forms and strategies categories along fine-scale hydromorphologic gradients in mountain streambeds was evaluated through multivariate statistical analysis and models. Frequency and abundance patterns suggested that species taxonomic groups and life forms and strategies categories distribution are mostly determined by the same microhabitat variables: water velocity, local light incidence and hydrologic zone in the streambed. Additionally, the distribution trends of each category are presented in graphic models summarizing the habitat segregation of bryophyte traits. The specificity of bryophyte distribution patterns were calibrated in undisturbed mountain watercourse to explore their use in monitoring fine-scale variation of flow and light regimes caused by anthropic influence. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction Since human impacts on biodiversity and habitats operate at different spatial and temporal scales, selections of the best indicators to observe changes over time and across scales of habitats are widely discussed (Carignan and Villard, 2002; Weber et al., 2004; Heino et al., 2005a). Moreover, a more integrative ecological perspective for environmental assessments and comprehensive type of biomonitoring is being explored through the use of functional or trait descriptors in freshwater ecology, in order to reflect the whole extent of human impact on complex ecological interactions (Karr, 1987; Ali et al., 1999; Willby et al., 2000). Riparian habitat and flow regime alterations are amongst the most frequent disturbances in rivers, which are quickly reflected in the diversity and structure of biological communities at local and microhabitat scales. At a finer scale, early and detailed evidences

∗ Corresponding author. Tel.: +351 220402790; fax: +351 220402799. E-mail addresses: [email protected], [email protected] (C. Vieira). 1470-160X/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecolind.2011.10.012

of flow and light changes can be measured through stream communities of organisms responsive at the microhabitat scale, such as bryophytes. As significant elements of freshwater biota, bryophytes show extremely specialized community structure and niche relationships (Suren, 1996; Heino et al., 2005b) and the zonation of their assemblages relative to stream water level has been reported in Europe (Gimingham and Birse, 1957; Muotka and Virtanen, 1995). Most stream bryophytes are ectohydric and grow directly on the rock surfaces as colonial populations and these, rather than the individual shoots, are their ecologically functional units, entirely dependent on the available water and climatic conditions (Bates, 1998). To colonize such demanding conditions, bryophytes show adaptations in their morphology, physiology and reproduction strategies, a result of convergent evolution from different terrestrial ancestors to the physical determinants of aquatic plant distribution (Vitt and Glime, 1984; Akiyama, 1995). Bryophyte functional classifications reflecting these convergence, such as life forms (Gimingham and Birse, 1957; Glime, 1968; Mägdefrau, 1982; Bates, 1998) and life strategies classifications (During, 1979; Grime et al.,

C. Vieira et al. / Ecological Indicators 18 (2012) 98–107

1990; During, 1992), remain valuable frameworks synthesizing and discussing the relationships between reproductive biology and ecological response of bryophytes in several habitats (Fritz et al., 2009; Oishi, 2009; Stehn et al., 2010). The ability of stream bryophytes to withstand seasonal desiccation and mechanical scouring is determined by the biotic resistance given by these shared adaptations which rule their changes in abundance and positioning in the streambed (Gimingham and Birse, 1957; Craw, 1976; Glime and Vitt, 1984; Biggs, 1996; Proctor, 2000). Nowadays, bryophyte life history information is becoming extensive (Dierssen, 2001; Ros et al., 2007) and species from stream communities can be thoroughly classified according to several trait classification schemes. Although bryophyte identification to a species level is a serious bottleneck during the surveying and quality assessment processes, broad recognition of bryophyte traits is realistic and possible to be accomplished in the field. Occurrence or absence of bryophyte growth forms and taxonomic or functional groups were indicated as useful indicators to interpret hydrologic permanence, especially in non-polluted mountain locations with stable substrates (Fritz et al., 2009). Currently, species data on bryophytes are collected in watercourse monitoring campaigns, as part of macrophyte protocols, so exploring the application of bryophyte features data could be a valuable investigation for improvement of stream assessments. According to some authors, a switch to the use of a smaller set of well-researched and calibrated indicator metrics would provide more meaningful data than the current “comprehensive” surveys of macrophytes, particularly when bryophytes are present (Lansdown and Bosanquet, 2010). This work focuses on the study of stream bryophyte communities, with many species common to near-natural mountain streams of European countries. By understanding which physical parameters relate more to which groups and traits, and the magnitude of such relationships, we submit that broad recognition of three Divisions of bryophytes and their life forms and life strategies, should be tested as a methodology to improve early detection of changes in mountain aquatic ecosystems. Since bryophyte classifications can be widely applied to any of the mountain stream communities in similar climatic and geomorphologic contexts, the potential indicator categories could have geographically broad application.

2. Methods 2.1. Study areas This survey was performed on watercourses included within the network of Natura 2000 Sites in two regions: (i) northwest region of Portugal, characterized by a strong and acid water flow in schist and granite bedrocks with temperate climate (700–3000 mm of total annual precipitation; 7–16 ◦ C of mean daily temperature) but with considerable intra-annual variability of stream discharge due to precipitation variation (maximum of 2 months of summer dryness when watercourses maintain a minimum water flow); and (ii) centre-west Portugal, characterized by limestone waterbeds with neutral water and longer dryness periods due to the lower levels of annual precipitation and influence of mediterranean climate (700–1400 mm of total annual precipitation; 12.6–16 ◦ C of mean daily temperature) (Fig. 1). Sampling was performed in mountain hills and valleys in altitudes ranging from 700 to 1440 m, corresponding to the headwater areas of many water basins. Here watercourses show typical features of high slope bedrock rivers with shifting currents and successions of pools and riffles, waterfalls and rapids.

99

Portuguese fluvial ecosystems present rich and diverse assemblages of bryophyte species, with greater value added by some taxa of great phytogeograghic importance related to colonization routes during the geologic history of the Iberian Peninsula (Sérgio, 1990) and to the refuge nature of this Peninsula during the last glacial age in late-Quaternary period (Petit et al., 2002). The tree species most frequently found in the northwest riparian ecosystems are Alnus glutinosa (L.) Gaertn., Betula celtiberica Rohtm et Vasc. and Salix atrocinerea Brot. Helophytic vegetation is usually composed ˜ & Aedo, Galof Carex elata All. subsp. reuteriana (Boiss.) Luceno ium broterianum Boiss. & Reuter, Viola palustris L. subsp. palustris, Oenanthe crocata L. and Osmunda regalis L. populations (Costa et al., 1998). In Portugal, mountain stream ecosystems also correspond to the microhabitats of many of the nationally threatened species (Vieira et al., 2004, 2005, 2007; Sérgio et al., 2006). 2.2. Sampling procedure and habitat variables Sampling was performed during 2002–2008, in 165 fluvial segments (defined as 100 m length of the watercourse and its margins) of several mountain ranges (Fig. 1). The surveys were performed during the lowest water discharge levels (late spring and summer–May to September), to access the constancy and levels of submergence. Depth was measured through visual assessments using a meter and bryophyte species abundance was registered as percentage cover using sample plots of 0.25 m2 (0.5 m × 0.5 m) placed in the hydrologic zones (HYDZON) recognizable according to Gilbert fluvial classification (Gilbert, 1996): (1) constantly submerged microhabitats under a water column deeper than 30 cm; (2) constantly submerged microhabitats with water depth between 30 and 10 cm; (3) constantly submerged microhabitats with 10 cm water depth maximum; (4) mesic microhabitats easily immersed several times a month with discharges related to precipitation or dam releases (typically 10–30 cm above minimum water level); (5) xeric microhabitats immersed seasonally with discharges related to precipitation or occasionally due to dam releases (typically 30–60 cm above minimum water level); (6) terrestrial microhabitats occasionally immersed by extended periods of rain (typically higher than 60 cm above minimum water level). In total, this survey resulted in 754 samples of fluvial microhabitats. Regional environmental variables for each fluvial segment were obtained with ArcGIS v. 9 from the Environmental Agency Maps (Agência Portuguesa do Ambiente, 2008) and 1:25,000 topographic maps and local and microhabitat hydrologic and geomorphologic aspects were determined in situ according to the classes defined in Table 1. 2.3. Data study and analysis Taxa nomenclature is according to Hill et al. (2006) and Ros et al. (2007) and authors’ abbreviations are those proposed by Brummit and Powell (1992) (Supporting Information). All specimens are deposited in Porto Herbarium (PO) in “CIBIO collection” with collection numbers ranging from 1221 to 10,306. Taxa locations and autoecology were published by Vieira et al. (Vieira et al., 2012). All bryophyte species were classified according to their taxonomic group (Division) in horworts (H), liverworts (L) or mosses (M) (Vanderpoorten and Goffinet, 2009) according to their field lifeforms through categories described by Glime (1968), Mägdefrau (1982) and Bates (1998) as annuals (An), short turfs (St), tall turfs (Tt), cushions (Cu); thalloid mats (tM), smooth mats (sM), rough mats (rM), fans (F), dendroids (D), streamers (S), wefts (W); and according to their life strategies following the concepts of During (1992) and the classification of Dier␤en (2001) as annual-shuttles (A), fugitives (Fu), ephemeral colonists (Ce), colonistc s.s. (C), pioneer colonists (Cp), short-lived shuttles (Ss), long-lived shuttles

100


Fig. 1. Geographical context of the studied area in Europe (a), in Iberian Peninsula (b) and Portugal (c) with sampling points (watercourse segments between 700 and 1440 m) over a representation Digital Elevation Terrain Model. NW: northwestern region (ULC: lat 41.81, long −8.87; LRC: lat 40.74, long −7.84); CW: centre-western region (ULC: lat 40.21, long −8.8751; LRC: lat 39.86, long −8.39) of Portugal.

(Ls), perennials s.s. (P), competitive perennials (Pc), stress tolerant perennials (Ps) (Supporting Information). Regional, local and microhabitat ecological variables correlation was analyzed through non-parametric Spearman correlation coefficients using PASW Statistics v.18.0.1 (IBM, 2009). Only

uncorrelated variables (Spearman‘s rho lower than |0.5| and significant at the 0.05 level (two-tailed)) were retained for further analysis (Table 1). The correlation between frequencies of taxonomic categories and taxa richness was explored through a Principal Component

Table 1 Code, weighted mean and numerical range of ecological variables measured at 165 mountain watercourses in the studied regions of Portugal. Variables

Code

Classmean (SD)

No. of classes

Real value range and class coding (in brackets)

Regional scale Mean air temperature (◦ C) Mean annual rainfall (mm)

TMART PRELP

1.98 (1.05) 3.67 (1.28)

4 6

7 (1) to 16 ◦ C (4) 700 (1) to 3000 mm (6)

Local scale (segment) Shading (class) Altitude (m)

CMAR ALTI

2.49 (1.58) 3.49 (1.35)

5 6

0 (1) to 100% (5) 600 (1) to 1500 m (6)

Micro-habitat Water turbulence (class) Substrate slope (%) Water velocity (m/s) Substrate dimension (cm) Hydrological zone (class)

TURB DECI VELO SUBS HYDZON

3.72 (0.91) 2.68 (1.28) 2.53 (1.57) 4.80 (1.70) 3.46 (0.88)

5 5 6 6 6

laminar (1) to turbulent (5) 0 (1) to 100% (5) 0 (1) to>5m/s (6) 1 mm (1) to rock slabs (6) constantly submerged (1) to mostly emerged with sediments (6)


101

Fig. 2. Percentage of occurrence of each category of taxonomic groups (1) life forms (2) and life strategies (3) in the considered submersion levels expressed as hydrologic zone (HYDZON – Table 1). Each of the concentric rings correspondents to the 6 classes of the variable hydrologic zone - interior rings are closer to the bottom of the streambed and exterior rings represent the zones less frequently submerged (Table 1). See Supporting Information for legends and explanations on bryophyte categories displayed.

Analysis (PCA). We focused scaling on inter-species correlations and a species centering/standardization was done, but no speciesweights were specified. In the PCA diagram, the categories were plotted in regard to their “Cfit” statistics, to explore the goodness of fitting of individual categories properties in the ordination model. The ecological variables were projected as passive co-variables in order to explore the correlation matrix with the ordination axes. The percentage coverage of the bryophytes with the same life form and life strategy categories was summed and converted to abundance-frequency values of Domin scale (Curral, 1987). This scale highlights the differences in coverage of uncommon or rare categories and reduces the emphasis of dominant categories (Jager and Looman, 1995). This coverage matrix and an environmental matrix were used in a Redundancy Analysis (RDA) to investigate how effectively bryophyte categories could be associated with the measured ecological gradients. No transformation of species data or species weighting were specified in the ordination, but a species centering/standardization was performed. The contribution of each variable to the RDA model was explored with automatic forward selection through conditional

effects and Monte-Carlo tests with unrestricted permutations (n = 499). Variables that contributed to the construction of each model at the 5% significance level were included in the order of their conditional effect. To explore the trends of richness of life functional categories in the ordination space and their relation to environmental parameters we performed “Locally Scatter plot Smoothing Models-Loess” on the number of categories present in each sample of RDA analysis based on least squares regressions (˛ = 0.67). To explore variation of individual functional categories response in respect to the most important variables specified in each RDA analysis we plotted the main trends of variation of each category using Generalized Linear Models (GLM), assuming Gaussian distributions and using Stepwise model selection with F-statistics (Threshold = 0.05). All ordination and modeling procedures were done with the software program CANOCO 4.5 (Ter Braak and ˇ Smilauer, 2003). We also summarized life forms and life strategies response along hydrologic and light gradients, through average value scatter plots, shown by each category for the two most determinant ecological variables pointed out by the RDA analysis.

102


Table 2 Micro-habitat, local and regional ecological values correlation matrix with first (AX1) and second (AX2) axes of Principal Component Analysis ordination diagram (Fig. 3). See Table 1 for explanations of ecological variables. Ecologic variable

AX1

AX2

Hydrological zones (HYDZON) Water velocity (VELO) Shading (CMAR) Water turbulence (TURB) Mean air temperature (TMART) Substrate dimension (SUBS) Mean annual rainfall (PRELP) Substrate slope (DECI) Altitude (ALTI)

0.335 −0.293 0.118 −0.088 −0.085 −0.041 0.059 0.086 0.029

0.090 −0.048 −0.081 0.014 0.070 0.032 −0.071 0.009 −0.094

3. Results 3.1. Taxonomic and functional richness and submersion patterns We found 163 taxa (77% mosses, 23% liverworts and one hornwort species) corresponding to about 23% of the total taxa listed for Portugal (Sérgio and Carvalho, 2003). Supporting Information lists the bryophyte species and their taxonomic groups, life forms and life strategies. More than 100 taxa occurred in three or more of the sampled streams, while 59 taxa occurred only once or twice. Average richness per plot was of 4.2, ranging from one to eighteen taxa per 0.25 m2 . Bryophytes were found in all the defined hydrologic zones (HYDZON) at different current velocities (0 to >5 m/s). About 25% of the taxa developed submerged under running water, but many of these species could also be found in zones intermittently submerged. In the total of observations, 75% corresponded to moss species, which were dominant in all the microhabitats but comparatively more abundant than liverworts or hornworts in the continuously submerged levels (HYDZON 1, 2 and 3) (Fig. 2(1)).

Fig. 4. Redundancy Analysis (RDA) of coverage values of life forms (1) and life strategies (2) in the studied watercourses (gray arrows) and ecological variables (black arrows). Dotted lines correspond to the isolines of the superimposed LOESS model representing the trends of variation of the number of functional categories of the samples in the ordination space. Axes eigenvalues - (Fig. 4(1)) AX1: 0.178; AX2: 0.089; (Fig. 5(2)) AX1: 0.046, AX2: 0.019. Cumulative percentage variance of species-environment relation (Fig. 4(1)): 83.3% (Fig. 4(2)): 78%. See Table 1 and Supporting Information for legends and explanations of ecological variables and categories displayed.

Fig. 3. Principal component analysis (PCA) of bryophyte taxa richness (ntaxa) and taxonomic groups frequencies (nH = number of hornworts; nL = number of liverworts; nM = number of mosses) in each of the studied watercourses. The diameter of circles in the diagram is proportional to how well the properties of individual entities are characterized by the fitted ordination model. Axis eigenvalues - AX1: 0.537; AX2: 0.24. Cumulative percentage variance of species data of first two axes: 77.8%; Cumulative percentage variance of species-environment relation: 84.3%. See Table 1 for legends and explanations of ecological variables.

We found eleven life-forms and ten life strategies amongst stream bryophytes. Life forms average number per sample was of 2.7 (ranging from one to the maximum of eight different life forms per sample), while an average number of 2.6 life strategies was found (ranging from one to the maximum of six different life strategies per sample). We found a clear dominance of smooth mats (sM = 37%), tall turfs (Tt = 25%), fans (F = 10%) and short turfs (St = 10%) life forms and perennials s.s. (P = 35%),


103

Table 3 Inclusion order of ecological variables in the Redundancy Analysis (RDA) models for life forms and life strategies distribution in the studied watercourses. Ecological variable (EV) correlation value (R) with RDA ordination first (AX1) and second (AX2) axes and their conditional effect evaluation (A). Variables are shown in the order of their inclusion in each of the RDA models. (n = 754 samples). See Table 1 for legends and explanations of ecologic variables. RDA life form model EV

HYDZON CMAR TURB DECI VELO PRELP SUBS ALTI TMART

RDA life strategies model

R

Conditional effect

EV

AX1

AX2

A

p

F

0.50 −0.16 −0.06 0.12 −0.48 −0.07 0.06 0.02 0.10

0.21 0.45 0.09 0.19 −0.06 0.28 −0.09 0.02 −0.32

0.05 0.03 0.01 0.01 0.01 0.01 0 0 0

0.002 0.002 0.002 0.018 0.002 0.002 0.090 0.004 0.004

35.66 25.90 4.98 2.23 11.75 6.53 1.64 3.68 2.48

VELO HYDZON CMAR ALTI SUBS PRELP DECI TURB TMART

R

Conditional effect

AX1

AX2

A

p

F

0.48 −0.43 0.07 0.01 −0.02 0.08 −0.12 0.11 −0.11

0.00 −0.03 −0.13 0.29 −0.07 0.08 −0.18 −0.01 −0.04

0.04 0.02 0.01 0.01 0.01 0 0 0 0

0.002 0.002 0.002 0.002 0.120 0.002 0.016 0.134 0.748

27.43 7.49 8.35 8.62 1.62 2.97 2.35 1.53 0.64

Fig. 5. Life forms (1 and 2) and life strategies (3 and 4) categories response trends of abundance (GLM individual models plotted as lines for each category) regarding the two most determinant ecological variables for their distribution as pointed by RDA models. See Table 1 and Supporting Information for legends and explanations of ecological variables and categories displayed.

104


competitive perennials (Pc = 22%) and colonists (C = 16%) life strategies (Fig. 2(2,3)). 3.2. Taxonomic categories correlations The PCA ordination analysis based on the number of observations of taxonomic categories and taxa richness in each microhabitat explained 77.8% of percentage variance in the first two axes (Fig. 3). The three taxonomic groups of bryophytes presented different trends of distribution in the samples with the increasing number of mosses (nM) and liverworts (nL) being associated with dissimilar ecological variables and hornworts (a group represented by less than five occurrences in the studied areas) placed in a very distinct area of the PCA biplot and not clearly correlated with any ecological variable. Moss richness (nM) was the variable most highly correlated with the richness of bryophyte taxa in a microhabitat. The individual categories best fitted in this PCA model were the number of taxa (ntaxa) present in each microhabitat, followed by the number of mosses (nM), which vary along the first axis. This axis was best regarded as a gradient determined mostly by the hydrologic zone and water velocity variables (Table 2). The number of liverworts per sample (nL) was mostly dependent on the higher levels of shading (CMAR), total precipitation (PRELP) and inclination of the substrate (DECI). 3.3. Functional categories models The construction of the RDA models with a forward selection methodology revealed different dynamics of inclusion and importance of variables. Nevertheless, the hydrologic zone (HYDZON) was consistently one of the most important variables in both models (Table 3). LOESS regression lines in the RDA diagram show a tendency of an increasing number of life forms and life strategies in microhabitats not so frequently submerged by fast running waters (Fig. 4(1,2)). 3.3.1. Life forms Life forms ordination model (Fig. 4(1)), showed a gradient of microhabitat assemblages going from those composed mainly by streamers (S), fans (F) and smooth mats (sM) to assemblages composed by a wider and different variety of the other life-forms. The projection of ecological variables could be adjusted to 83% of the variance of categories-variables relation in the first two axes. The first axis gradient was mostly associated with the hydrologic zone (HYDZON = 0.05, p < 0.05) and shading effects (CMAR = 0.03, p < 0.05) (Table 3). RDA analysis (Fig. 4(1)) and life-forms individual response trends (Fig. 5(1,2) and Fig. 6(1)), confirmed that streamers (S) and smooth mats (sM) were associated with more deeply submerged sites, although they differ in their tolerance to light incidence. All the other life forms seemed to develop better in emerged positions, where richness of life-forms is higher (Fig. 4(1)). Lower light conditions seemed to favour the development of thalloid and smooth mats, fans and dendroids which are also correlated with higher precipitation values (PRELP) as displayed along the second axis of the RDA biplot (Fig. 4(1)). 3.3.2. Life strategies The first two constrained axes of the RDA analysis display 78.7% of the percentage variance of species-environment in life strategies biplot (Fig. 4(2)). Water velocity (VELO = 0.04, p < 0.05) and the hydrologic zone (HYDZON = 0.02, p < 0.05) were the most influential ecological variables (Table 3), segregating along the first axis the communities composed mostly of perennials (P) or ephemeral colonists (Ce) from the communities richer in all the other life

strategies occurring in sites with slower currents or emergent positions. At these less frequently immerged hydrologic zones the number of life strategies also increased (Fig. 4(2)). The second axis revealed a weaker gradient associated with altitude (ALTI), which seemed to favour the presence of competitive perennials (Pc). Response trends of life strategies categories (Fig. 5(3,4) and Fig. 6(2)) showed that perennials (P) are favoured by permanent fast-flowing currents, while pioneer colonists (Cp) and colonists (C) are favoured in the lower currents or emerged positions.

4. Discussion The usefulness of taxonomic groups and functional traits as indicators of hydrologic permanence, as explored by Fritz et al. (2009), was extended in this study by interpreting the influence of other synergetic ecological variables in the segregation of bryophyte groups in streambeds. Taxonomic and functional categories distribution along the stream microhabitats gradients correlated in a small extent to regional variables and more strongly with fine scale variables such as the position of the microhabitat in relation to the water level (HYDZON), shading (CMAR) and water velocity (VELO) (Tables 2 and 3; Figs. 4 and 5). These results are analogous to other studies that emphasized the importance of the moisture supply (Gimingham and Birse, 1957), water drag forces (Suren et al., 2000) and light incidence (Birse, 1958) as major environmental drivers for bryophyte communities composition and structure. The patterns of segregation of bryophyte traits along submergence and water velocity gradients observed in the field can also be correlated with the disturbance caused by the movement of the water (Kimmerer and Allen, 1982; Slack and Glime, 1985; Muotka and Virtanen, 1995). The organization of bryophyte populations in overlapping bands is specially characteristic of southern Europe streams with highly fluctuating water levels and regular seasonal desiccation periods caused by the particular flow regimes (Bowden et al., 1999). Our PCA analysis and LOESS regression models (Figs. 3 and 4) showed that taxonomic and functional richness increases in less frequently submerged habitats (HYDZON 4–6). In the studied areas, these corresponded to stream margins and boulders, zones with stable drippings and splashes where occasional flood disturbance creates gaps, maintaining high taxa richness through new colonizers (Kimmerer and Allen, 1982; Englund, 1991; Steinman and Boston, 1993; Muotka and Virtanen, 1995). Moreover, the large increase of species in these microhabitats is particularly evident in shaded conditions, where the combination of controlled radiation and moisture is optimal for many bryophytes to grow (Bergamini et al., 2001). Therefore, taxonomic and functional richness might be indicators of water level and velocity, since these tend to be lower in more continuously submerged microhabitats where dense monospecific colonies of the few truly aquatic species or truly hydrodynamic species tend to prevail (Vitt and Glime, 1984; Muotka and Virtanen, 1995; Fritz et al., 2009).

4.1. Taxonomic groups and species richness The maximum bryophyte richness is achieved through the colonization with species of mosses in all studied micro-habitats (Fig. 2(1)). The higher values of bryophyte and moss richness can be interpreted as signs of a hydrologic zone less frequently submerged by fast waters (Fig. 3). This tendency of higher bryophyte species richness in zones of watercourses with intermediate levels disturbance or in ephemeral stretches or was also shown by Fritz et al. (2009).


105

4.2. Life forms Life forms of mosses clearly present better adaptations to seasonal desiccation and dragging forces either in permanent submersion or flood events, with a firmer structure able to resist to mechanical forces (Vitt and Glime, 1984; Muotka and Virtanen, 1995; Fritz et al., 2009). With the exception of some liverwort foliose smooth mats, most of the liverwort thalloid species could only be found in seasonally immersed or splashed margins deeply shaded throughout the year. These are known to be intolerant to the physiologic stress caused by continuous submersion, drought or mechanical scouring (Gimingham and Birse, 1957; Kimmerer and Allen, 1982; Martinez-Abaigar and NunezOlivera, 1991). In our study their abundant presence was a sign of more humid and shaded conditions and of the upper limit of flooding waters impact, above which these thalloid species develop. Taxa developing in permanently submerged levels were commonly foliose species with reduced and prostrate smooth surface areas. These corresponded mostly to streamers (S) (dangling forms sensu Glime (1968)) and smooth mats (sM), found up to 30 cm of depth (HYDZON 1 and 2), demonstrating the biological relevance of these life forms within the spectrum of submerged communities (Fig. 2(2)). These two life forms have been designated as dissimilar strategies of surface area and CO2 uptake in aquatic bryophytes living at different water velocities, depths and irradiance situations (Birse, 1958; Jenkins and Proctor, 1985). In fact, we found streamers mostly on slower currents of streambed in full sunlight, while smooth mats were most easily found in torrential water impact zones in deep shaded microhabitats (Fig. 5(1)). Microhabitats with frequent water level fluctuations and closer to water (HYDZON 3) usually correspond to a higher presence of bryophytes with tri-dimensional life forms resistant to desiccation and dragging forces (Fig. 2(2)). Well anchored fans, dendroids and short turfs were frequently found in the vertical surfaces of rocks at short distances from water, in splashed zones. These rather different life forms correspond to different tactics either to reduce exposure area to current, namely the distichous leaf arrangement of fans and secondary branches of dendroids or the short compact form of short-turfs (Vitt and Glime, 1984). Moreover, frequently splashed or dripping zones that are never subjected to torrential flow can be identified in shaded places by the presence of desiccation-sensitive fleshy leafy or thalloid mats of liverworts and hornworts, intolerant to elevated drag coefficients and long periods of submersion. In lighted situations, the tall turfs with high biomass and dense colonies avoid photo-inhibition through self-shading (Bates, 1998) can be used as indicators of the constant splash or dripping zones which are never severely submerged. The microhabitats usually subjected to seasonal floods with strong impact of water (HYDZON 4 and 5) are recognizable when colonized by tall and open turfs that, despite not being very hydrodynamic resist, both to desiccation and water abrasion, through their stiff texture given by multi-layer tissues and thick wall cells (Vitt and Glime, 1984). The upper zones of stone surfaces less frequently subjected to strong currents (HYDZON 6), in exposed streambeds, were colonized by smooth densely-packed cushions or short turfs resistant to drought stress (Gimingham and Birse, 1957; Muotka and Virtanen, 1995; Barrat-Segretain, 1996). In this same top or higher zones of the boulders, but if shaded conditions prevail for most of the year, emerged smooth mats developed along with fans (Fig. 5(1) and Fig. 6(1)). Additionally, microhabitats higher than the normal level of maximum floods could be recognized by the co-existence annuals, loose rough mats or wefts that developed mostly associated with deposited sediments.

Fig. 6. Life forms (1) and life strategies (2) summary models regarding gradients composed of two most determinant ecological variables – each category is located in its average value concerning the variation of each variable. See Table 1 and Supporting Information for legends and explanations of ecological variables and categories displayed.

4.3. Life strategies The general influence of water velocity, frequency of submersion and the disturbance associated with these two factors on the strategies of development and reproduction was verified in our work. The overall predominance of perennials in the studied segments was indicative of the regularity of ecological conditions (During, 1979; Lloret, 1986), which corresponds, in our case, to the regularity of the hydrologic regimes. The constancy of water presence and the demands of adaptation to rapid currents at the submerged levels (HYDZON 1 and 2 with high water velocity) originated low diversity communities composed of perennials

106


(perennials s.s. or competitive perennials). We frequently observed colonial growth accomplished by shoot innovations firmly attached to the substrate, assuring the longevity of the population under the column of water (During, 1990; Grime et al.,1990; Muotka and Virtanen, 1995). Therefore, persistency of these patches of perennials could be used as indicators of zones of steady and fast-flowing discharge patterns. Ephemeral colonists indicated the stream zones submerged by shifting and very fast abrasive currents (HYDZON 1 and 2), since they were typically found colonizing minute rock crevices in the first succession stages under the most torrential currents (Muotka and Virtanen, 1995). On the other hand, colonists and pioneer colonists, positively correlated with a moderate distance to the water presence and impact (Fig. 4(2), Fig. 5(3,4)), indicated the zones flooded seasonally with strong discharges (HYDZON 3–4). As species typical of secondary succession series in substrates strongly eroded, dragged or recently deposited during high flow events, these high disturbance-dependent life strategies reflected the unpredictability of environmental conditions of streambeds, in space and time (During, 1979; Kimmerer and Allen, 1982). In microhabitats emerged for brief periods in each season, we found fugitives, annual shuttles and stress tolerant perennials, mostly terricolous species taking their opportunity to colonize some deposited sediments. The dominance of opportunistic annual and fugitive species reflected the unpredictability occurrence of higher level of nutrients in earlier secondary succession stages (During, 1979; Kimmerer and Allen, 1982; Bates, 1998). The presence of short-lived or long-lived shuttle species, typically in microhabitats distant from water level (HYDZON 4–6), might be indicative of the zones of erosion caused by sporadic disturbance. These species strategies allow them to develop in micro-habitats stable for few to some years, until sporadic flooding or substrate movement events occur and destroy their populations. 4.4. Gradient models Substitution of life forms and life strategies along hydrologic and light gradients becomes obvious with the scatter plots based on the average values shown by each category regarding the most determinant ecological variables (Fig. 6(1,2)). Life-form scatter plot obtained through our study confirmed the theoretical model by Bates (1998), devised with water proximity (as moisture availability) and shading (as irradiance) variables as determinants of bryophyte life form segregation in hard substrata. 5. Conclusions Our findings confirmed that the mechanical and physiological constrains imposed by drag forces and length of submersion periods, along with the amount of incident light, segregate aquatic and semi-aquatic bryophyte populations according to their traits, with a clear substitution of dissimilar resisting forms along hydrologic and micro-climatic gradients (Fig. 6(1,2)). Since bryophytes are sessile and the only plants critically dependent upon the water column, they reflect conditions in a particular stretch of river and provide an integrated record of seasonal or disturbance factors on their growth, being amongst the most reliable water pollution indicators (Vanderpoorten, 2002; Zechmeister et al., 2003). The consistency and specificity of ecological determination of bryophytes traits in streams suggests the potential use of some of their taxonomic and functional categories as quick responsive metrics and fine-scale indicators in monitoring hydrologic and micro-climatic pressures on stream ecosystems. Bryophytes, being conspicuous elements of mountain reaches, can fulfil the lack of information by indicators such as vascular macrophytes where or

when these are not so abundant or there are methodological and budget constrains associated with the use of fishes or other animals as indicators, usually more suitable for a higher scale monitoring. Together with the extensive auto-ecology survey of bryophyte communities (Vieira et al., 2012), this work presents the first approach to Portuguese aquatic bryophytes diversity, life forms and strategies. In this context, it constitutes the first investigation on the possibility of inference of prevailing conditions at the microhabitats level. This work proposes to be the reference for subsequent studies in mountain streams that evaluate hydrological disturbances or changes in irradiance in the streambed through bryophytic functional and taxonomic information at European level. Acknowledgements We thank Foundation for Science and Technology (FCT), for providing funding through doctoral and post-doc grants (SFRH/BD/6969/2001; SFRH/BPD/63741/2009) to the first author. We also acknowledge the financial support of the “SYNTHESYS Project” for the study of “Aquatic and semi-aquatic Bryophytes from Europe harboured at the Museum National d’HistoireNaturelle and interactions processes between bryophytes and water quality (bioindication and bioaccumulation)”, in MNHM (Paris–France). Thanks also to two anonymous reviewers for comments and corrections on the previous version of the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ecolind.2011.10.012. References Agência Portuguesa do Ambiente (APA), 2008. Atlas do Ambiente (Maps I.16.4, I.13, I.9, I.6, I.1, I.4.1, III.1, I.2). Available at: http://www.iambiente.pt/atlas/est/index.jsp. Accessed 12 July 2008. Akiyama, H., 1995. Rheophytic mosses: their morphological, physiological, and ecological adaptations. Acta Phytotax. Geobot. 46, 77–98. Ali, M.M., Murphy, K.J., Abernethy, V.J., 1999. Macrophyte functional variables versus species assemblages as predictors of trophic status in flowing waters. Hydrobiologia 415, 131–138. Barrat-Segretain, M.H., 1996. Strategies of reproduction, dispersion, and competition in river plants: a review. Vegetatio 123, 13–37. Bates, J.W., 1998. Is life-form a useful concept in bryophyte ecology? Oikos 82, 233–237. Bergamini, A., Pauli, D., Peintinger, M., Schmid, B., 2001. Relationship between productivity, number of shoots and number of species in bryophytes and vascular plants. J. Ecol. 89, 920–929. Biggs, B.J.F., 1996. Hydraulic habitat of plants in streams. Regul. Rivers: Res. Manage. 12, 131–144. Birse, E.M., 1958. Ecological studies on growth-form in Bryophytes. III. The relationship between the growth-form and ground water supply. J. Ecol. 46, 9–27. Bowden, W.B., Arscott, D.B., Pappathanasi, D., Finlay, J.C., Glime, J.M., Lacroix, J., Liao, C.L., Hershey, A., Lampella, T., Peterson, B., Wollheim, W., Slavik, K., Shelley, B., Chesterton, M.B., Lachance, J.A., Leblanc, R.M., Steinman, M., Suren, A.M., Stream Bryophyte Group, 1999. Roles of bryophytes in stream ecosystems. J. North Am. Bentholog. Soc. 18, 151–184. Brummit, R.K., Powell, C.E., 1992. Authors of plant names. Kew, Royal Botanic Gardens. Carignan, V., Villard, M.-A., 2002. Selecting indicator species to monitor ecological integrity: a review. Environ. Monit. Assess. 78, 45–61. Costa, J.C., Aguiar, C., Capelo, J.H., Lousã, M., Neto, C., 1998. Biogeografia de Portugal Continental. Quercetea, 5–56. Craw, R.C., 1976. Streamside bryophyte zonations. N Z J. Botany 14, 19–28. Curral, J.E.P., 1987. A transformation of the Domin scale. Vegetatio 72, 81–87. Dierssen, K., 2001. Distribution, Ecological Amplitude and Phytosociological Characterization of European Bryophytes. J. Cramer, Berlin. During, H.J., 1979. Life strategies of bryophytes: a preliminary review. Lindbergia 5, 2–18. During, H.J., 1990. Clonal Growth Patterns Among Bryophytes. In: Kroon, J. (Ed.), Clonal Growth in Plants: Regulation and Function. SPB Academic Publishing, pp. 153–176. During, H.J., 1992. Ecological Classifications of Bryophytes and Lichens. In: Bates, J.W., Farmer, A.M. (Eds.), Bryophytes and Lichens in a Changing Environment. Claredon Press, Oxford, PP. 1–25.

C. Vieira et al. / Ecological Indicators 18 (2012) 98–107 Englund, G., 1991. Effects of disturbance on stream moss and invertebrate community structure. J. North Am. Bentholog. Soc. 10, 143–153. Fritz, K.M., Glime, J., Hribljan, J., Greenwood, J.L., 2009. Can bryophytes be used to characterize hydrologic permanence in forested headwater streams? Ecol. Ind. 9, 681–692. Gilbert, O.L., 1996. The lichen vegetation of chalk and limestone streams in Britain. Lichenologist 28, 145–159. Gimingham, C.H., Birse, E.M., 1957. Ecological studies on growth-form in bryophytes: correlations between growth forms and habitat. J. Ecology 45, 533–545. Glime, J.M., 1968. Ecological observations on some bryophytes in Appalachian mountain streams. Castanea 33, 300–325. Glime, J.M., Vitt, D.H., 1984. The physiological adaptations of aquatic Musci. Lindbergia 10, 41–52. Grime, J.P., Rincon, E.R., Wickerson, B.E., 1990. Bryophytes and plant strategy theory. Bot. J. Linn. Soc. 104, 175–186. Heino, J., Paavola, R., Virtanen, R., Muotka, T., 2005a. Searching for biodiversity indicators in running waters: do bryophytes, macroinvertebrates, and fish show congruent diversity patterns? Biodiv. Conserv. 14, 415–428. Heino, J., Virtanen, R., Vuori, K.-M., Saastamoinen, J., Ohtonen, A., Muotka, T., 2005b. Spring bryophytes in forested landscapes: land use effects on bryophyte species richness, community structure and persistence. Biol. Conserv. 124, 539–545. Hill, M.O., Bell, N., Bruggeman-Nannenga, M.A., Brugués, M., Cano, M.J., Enroth, J., Flatberg, K.I., Frahm, J.-P., Gallego, M.T., Garilleti, R., Guerra, J., Hedenäs, L., ˜ Holoyak, D.T., Hyvönen, J., Ignatov, M.S., Lara, F., Mazimpaka, V., Munoz, J., Söderström, L., 2006. Bryological monograph. An annotated checklist of the mosses of Europe and Macaronesia. J. Bryology 28, 198–267. IBM, 2009. PAWS STATISTICS v. 18.0.1. IBM. Jager, J.C., Looman, C.W.N., 1995. Data Collection. In: Jongman, R.H.G., ter Braak, C.J.F., van Tongeren, O.F.R. (Eds.), Data Analysis in Community and Landscape Ecology. Cambridge University Press, Cambridge, pp. 10–28. Jenkins, J.T., Proctor, M.C.F., 1985. Water-velocity, growth-form and diffusion resistances to photosynthetic CO2 uptake in aquatic bryophytes. Plant Cell Environ. 8, 317–323. Karr, J.R., 1987. Biological monitoring and environmental assessment: a conceptual framework. Environ. Manage. 11, 249–256. Kimmerer, R.W., Allen, T.F.H., 1982. The role of disturbance in the pattern of a riparian bryophyte community. Am. Midland Nat. 107, 370–383. Lansdown, R., Bosanquet, S., 2010. Riverine Plants as Biological Indicators. In: Hurford, C., Schneider, M., Cowx, I. (Eds.), Conservation Monitoring in Freshwater Habitats: A Practical Guide and Case Studies. Springer, pp. 73–84. Lloret, F., 1986. La vegetación rupícola en relación con los gradientes altitudinal e hígrico en el Montseny (Barcelona). Orsis 2, 55–70. Mägdefrau, K., 1982. Life-Forms of Bryophytes. In: Smith, A.J.E. (Ed.), Bryophyte Ecology. Chapman & Hall, London, pp. 45–59. ˜ Martínez-Abaigar, J., Núnez-Olivera, E., 1991. Briófitos acuáticos del río Iregua (La Rioja) - Estudio florístico, ecológico y ecofisiológico. Respuestas a la contaminación orgánica. Gobierno de La Rioja, Instituto de Estudios Riojanos. Muotka, T., Virtanen, R., 1995. The stream as a habitat templet for bryophytes: species’ distributions along gradients in disturbance and substratum heterogeneity. Freshwater Biol. 33, 141–160. Oishi, Y., 2009. A survey method for evaluating drought-sensitive bryophytes in fragmented forests: a bryophyte life-form based approach. Biol. Conserv. 142, 2854–2861. Petit, R.J., Brewer, S., Bordacs, S., Burg, K., Cheddadi, R., Coart, E., Cottrell, J., Csaikl, U.M., Van Dam, B., Deans, J.D., Espinel, S., Fineschi, S., Finkeldey, R., Glaz, I., Goicoechea, P.G., Jensen, J.S., Konig, A.O., Lowe, A.J., Madsen, S.F., Matyas, G., Munro, R.C., Popescu, F., Slade, D., Tabbener, H., De Vries, S.G.M., Ziegenhagen, B., De Beaulieu, J.L., Kremer, A., 2002. Identification of refugia and post-glacial

View publication stats

107

colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol. Manage. 156, 49–74. Proctor, M.C.F., 2000. The bryophyte paradox: tolerance of desiccation, evasion and drought. Plant Ecol. 151, 41–49. Ros, R.M., Mazimpaka, V., Abou-Salama, U., Aleffi, M., Blockeel, T.L., Brugués, M., Cano, M.J., Cros, R.M., Dia, M.G., Dirkse, G.M., Saadawi, W.E., Erda, A., Ganeva, A., González-Mancebo, J.M., Herrnstadt, I., Khalil, K., Kürschner, H., ˜ Lanfranco, E., Losada-Lima, A., Refai, M.S., Rodríguez-Nunez, S., Sabovljevi, M., Sérgio, C., Shabbara, H., Sim-Sim, M., Söderström, L., 2007. Hepatics and anthocerotes of the Mediterranean, an annotated checklist. Cryptogamie Bryologie 28, 351–437. Sérgio, C., 1990. Perspectiva biogeográfica da flora briológica Ibérica. Anales del Jardín Botánico de Madrid 46, 371–392. Sérgio, C., Brugés, M., Cros, R.M., Casas, C., Garcia, C., 2006. The 2006 Red List and updated checklist of bryophytes of the Iberian Peninsula (Portugal, Spain and Andorra). Lindbergia 31, 109–125. Sérgio, C., Carvalho, S., 2003. Annotated catalogue of Portuguese bryophytes. Portugaliae Acta Biologica 21, 5–230. Slack, N.G., Glime, J.M., 1985. Niche relationships of mountain stream bryophytes. The Bryologist 88, 7–18. Stehn, S.E., Webster, C.R., Glime, J.M., Jenkins, M.A., 2010. Elevational gradients of bryophyte diversity, life forms, and community assemblage in the southern Appalachian Mountains. Can. J. Forest Res. 40, 2164–2174. Steinman, A.D., Boston, H.L., 1993. The ecological role of aquatic bryophytes in a heterotrophic woodland stream. J. North Am. Bentholog. Soc. 12, 17–26. Suren, A.M., 1996. Bryophyte distribution patterns in relation to macro-, meso, and micro-scale variables in South Island, New Zealand streams. N Z J. Marine Freshwater Res. 30, 501–523. Suren, A.M., Smart, G.M., Smith, R.A., Brown, S.L.R., 2000. Drag coefficients of stream bryophytes: experimental determinations and ecological significance. Freshwater Biol. 45, 309–317. ˇ Ter Braak, C.J.F., Smilauer, P., 2003. Canoco 4.52 for Windows, Biometris. Plant research International, Wageningen, The Netherlands. Vanderpoorten, A., 2002. Hydrochemical Determinism, Ecological Polymorphism, and Indicator Values of Aquatic Bryophytes for Water Quality. In: Ambasht, R.S., Ambasht, N.K. (Eds.), Applied Aquatic Ecology. Modern Trends in Ecology & Environment. Kluwer Academic Publishers, New York, pp. 65–96. Vanderpoorten, A., Goffinet, B., 2009. Introduction to Bryophytes. Cambridge University Press, Cambridge. Vieira, C., Luís, L., Séneca, A., Sim-Sim, M., Sérgio, C., 2004. New national and regional bryophyte records: Radula holtii spruce. J. Bryology 26, 307. Vieira, C., Séneca, A., Sérgio, C., 2005. Threatened bryophytes occurence in Por˜ tuguese stream habitat. Boletín de la Sociedad Espanola de Bríologia. 26–27, 103–118. Vieira, C., Sérgio, C., Séneca, A., 2007. Some remarkable bryophytes from the aquatic habitats of the northwest of Portugal. Cryptogamie Bryologie 28, 1–8. Vieira, C., Séneca, A., Sérgio, C., 2012. Floristic and ecologic survey of bryophytes from portuguese watercourses. Cryptogamie Bryol. 33 (1.), in press. Vitt, D.H., Glime, J.M., 1984. The structural adaptations of aquatic Musci. Lindbergia 10, 95–110. Weber, D., Hintermann, U., Zangger, A., 2004. Scale and trends in species richness: considerations for monitoring biological diversity for political purposes. Global Ecol. Biogeogr. 13, 97–104. Willby, N.J., Abernethy, V.J., Demars, B.O.L., 2000. Attribute-based classification of European hydrophytes and its relationship to habitat utilization. Freshwater Biol. 43, 43–74. Zechmeister, H.G., Grodzinska, K., Szarek-Lukazewska, S., 2003. Bioindicators in Use: Bryophytes. In: Markert, B.A., Breure, A.M., Zechmeister, H.G. (Eds.), Bioindicators and Biomonitors: Principles, Concepts and Applications. Elsevier, pp. 329–376.